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Cited by 214Retinal Development and DisordersDevelopmental Biology and Gene RegulationRetinoids in leukemia and cellular processes

Regulation of photoreceptor gene expression by Crx-associated transcription factor network

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Hennig, Anne K., Peng, Guang-Hua, Chen, Shiming·2008·Brain Research
DOI 10.1016/j.brainres.2007.06.036PMC PMC2266892
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Abstract

Rod and cone photoreceptors in the mammalian retina are special types of neurons that are responsible for phototransduction, the first step of vision. Development and maintenance of photoreceptors require precisely regulated gene expression. This regulation is mediated by a network of photoreceptor transcription factors centered on Crx, an Otx-like homeodomain transcription factor. The cell type (subtype) specificity of this network is governed by factors that are preferentially expressed by rods or cones or both, including the rod-determining factors neural retina leucine zipper protein (Nrl) and the orphan nuclear receptor Nr2e3; and cone-determining factors, mostly nuclear receptor family members. The best-documented of these include thyroid hormone receptor beta2 (Tr beta2), retinoid related orphan receptor Ror beta, and retinoid X receptor Rxr gamma. The appropriate function of this network also depends on general transcription factors and cofactors that are ubiquitously expressed, such as the Sp zinc finger transcription factors and STAGA co-activator complexes. These cell type-specific and general transcription regulators form complex interactomes; mutations that interfere with any of the interactions can cause photoreceptor development defects or degeneration. In this manuscript, we review recent progress on the roles of various photoreceptor transcription factors and interactions in photoreceptor subtype development. We also provide evidence of auto-, para-, and feedback regulation among these factors at the transcriptional level. These protein-protein and protein-promoter interactions provide precision and specificity in controlling photoreceptor subtype-specific gene expression, development, and survival. Understanding these interactions may provide insights to more effective therapeutic interventions for photoreceptor diseases.

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  • Certain differentiation gene batteries composed of orthologous effector genes and the regulatory state drivers that activate them are known in all bilaterian animals investigated and even in cnidarians, e.g., in muscle cells, neurons, photoreceptor cells, and neurosecretory cells.

    “Certain differentiation gene batteries composed of orthologous effector genes and the regulatory state drivers that activate them are known in all bilaterian animals investigated and even in cnidarians, e.g., in muscle cells (5) neurons (13), photoreceptor cells (14 -17), and neurosecretory cells (17).”

    From Transphyletic conservation of developmental regulatory state in animal evolution (2011) · cites this paper as [14]

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References 158 · Cited by 214

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  1. Acampora D, Mazan S, Lallemand Y, Avantaggiato V, Maury M, Simeone A, Brulet P. Forebrain and midbrain regions are deleted in Otx2−/− mutants due to a defective anterior neuroectoderm specification during gastrulation. Development. 1995;121:3279–3290. doi: 10.1242/dev.121.10.3279. [DOI] [PubMed] [Google Scholar] · DOI
  2. Acharya HR, Dooley CM, Thoreson WB, Ahmad I. cDNA cloning and expression analysis of NeuroD mRNA in human retina. Biochem Biophys Res Commun. 1997;233:459–463. doi: 10.1006/bbrc.1997.6483. [DOI] [PubMed] [Google Scholar] · DOI
  3. Akagi T, Mandai M, Ooto S, Hirami Y, Osakada F, Kageyama R, Yoshimura N, Takahashi M. Otx2 homeobox gene induces photoreceptor-specific phenotypes in cells derived from adult iris and ciliary tissue. Invest Ophthalmol Vis Sci. 2004;45:4570–4575. doi: 10.1167/iovs.04-0697. [DOI] [PubMed] [Google Scholar] · DOI
  4. Akagi T, Akita J, Haruta M, Suzuki T, Honda Y, Inoue T, Yoshiura S, Kageyama R, Yatsu T, Yamada M, Takahashi M. Iris-derived cells from adult rodents and primates adopt photoreceptor-specific phenotypes. Invest Ophthalmol Vis Sci. 2005;46:3411–3419. doi: 10.1167/iovs.04-1112. [DOI] [PubMed] [Google Scholar] · DOI
  5. Akimoto M, Cheng H, Zhu D, Brzezinski JA, Khanna R, Filippova E, Oh EC, Jing Y, Linares JL, Brooks M, Zareparsi S, Mears AJ, Hero A, Glaser T, Swaroop A. Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors. Proc Natl Acad Sci U S A. 2006;103:3890–3895. doi: 10.1073/pnas.0508214103. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  6. Andre E, Gawlas K, Becker-Andre M. A novel isoform of the orphan nuclear receptor RORbeta is specifically expressed in pineal gland and retina. Gene. 1998;216:277–283. doi: 10.1016/s0378-1119(98)00348-5. [DOI] [PubMed] [Google Scholar] · DOI
  7. Ang SL, Jin O, Rhinn M, Daigle N, Stevenson L, Rossant J. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development. 1996;122:243–252. doi: 10.1242/dev.122.1.243. [DOI] [PubMed] [Google Scholar] · DOI
  8. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krzystolik MG, Lyass LA, Robbins JT. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron. 2000;27:513–523. doi: 10.1016/s0896-6273(00)00062-3. [DOI] [PubMed] [Google Scholar] · DOI
  9. Azadi S, Zhang Y, Caffe AR, Holmqvist B, van Veen T. Thyroid-beta2 and the retinoid RAR-alpha, RXR-gamma and ROR-beta2 receptor mRNAs; expression profiles in mouse retina, retinal explants and neocortex. Neuroreport. 2002;13:745–750. doi: 10.1097/00001756-200205070-00003. [DOI] [PubMed] [Google Scholar] · DOI
  10. Baas D, Bumsted KM, Martinez JA, Vaccarino FM, Wikler KC, Barnstable CJ. The subcellular localization of Otx2 is cell-type specific and developmentally regulated in the mouse retina. Brain Res Mol Brain Res. 2000;78:26–37. doi: 10.1016/s0169-328x(00)00060-7. [DOI] [PubMed] [Google Scholar] · DOI
  11. Baird-Titus JM, Clark-Baldwin K, Dave V, Caperelli CA, Ma J, Rance M. The solution structure of the native K50 Bicoid homeodomain bound to the consensus TAATCC DNA-binding site. J Mol Biol. 2006;356:1137–1151. doi: 10.1016/j.jmb.2005.12.007. [DOI] [PubMed] [Google Scholar] · DOI
  12. Bessant DA, Payne AM, Mitton KP, Wang QL, Swain PK, Plant C, Bird AC, Zack DJ, Swaroop A, Bhattacharya SS. A mutation in NRL is associated with autosomal dominant retinitis pigmentosa. Nat Genet. 1999;21:355–356. doi: 10.1038/7678. [DOI] [PubMed] [Google Scholar] · DOI
  13. Bibb LC, Holt JK, Tarttelin EE, Hodges MD, Gregory-Evans K, Rutherford A, Lucas RJ, Sowden JC, Gregory-Evans CY. Temporal and spatial expression patterns of the CRX transcription factor and its downstream targets. Critical differences during human and mouse eye development. Hum Mol Genet. 2001;10:1571–1579. doi: 10.1093/hmg/10.15.1571. [DOI] [PubMed] [Google Scholar] · DOI
  14. Blackshaw S, Fraioli RE, Furukawa T, Cepko CL. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell. 2001;107:579–589. doi: 10.1016/s0092-8674(01)00574-8. [DOI] [PubMed] [Google Scholar] · DOI
  15. Bobola N, Briata P, Ilengo C, Rosatto N, Craft C, Corte G, Ravazzolo R. OTX2 homeodomain protein binds a DNA element necessary for interphotoreceptor retinoid binding protein gene expression. Mech Dev. 1999;82:165–169. doi: 10.1016/s0925-4773(98)00162-2. [DOI] [PubMed] [Google Scholar] · DOI
  16. Bovolenta P, Mallamaci A, Briata P, Corte G, Boncinelli E. Implication of OTX2 in pigment epithelium determination and neural retina differentiation. J Neurosci. 1997;17:4243–4252. doi: 10.1523/JNEUROSCI.17-11-04243.1997. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  17. Bowes C, van Veen T, Farber DB. Opsin, G-protein and 48-kDa protein in normal and rd mouse retinas: developmental expression of mRNAs and proteins and light/dark cycling of mRNAs. Exp Eye Res. 1988;47:369–390. doi: 10.1016/0014-4835(88)90049-8. [DOI] [PubMed] [Google Scholar] · DOI
  18. Bumsted O'Brien KM, Cheng H, Jiang Y, Schulte D, Swaroop A, Hendrickson AE. Expression of photoreceptor-specific nuclear receptor NR2E3 in rod photoreceptors of fetal human retina. Invest Ophthalmol Vis Sci. 2004;45:2807–2812. doi: 10.1167/iovs.03-1317. [DOI] [PubMed] [Google Scholar] · DOI
  19. Carter-Dawson LD, LaVail MM. Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J Comp Neurol. 1979;188:263–272. doi: 10.1002/cne.901880205. [DOI] [PubMed] [Google Scholar] · DOI
  20. Cepko CL. The patterning and onset of opsin expression in vertebrate retinae. Curr Opin Neurobiol. 1996;6:542–546. doi: 10.1016/s0959-4388(96)80062-6. [DOI] [PubMed] [Google Scholar] · DOI
  21. Cepko C. Giving in to the blues. Nat Genet. 2000;24:99–100. doi: 10.1038/72887. [DOI] [PubMed] [Google Scholar] · DOI
  22. Chatelain G, Fossat N, Brun G, Lamonerie T. Molecular dissection reveals decreased activity and not dominant negative effect in human OTX2 mutants. J Mol Med. 2006;84:604–615. doi: 10.1007/s00109-006-0048-2. [DOI] [PubMed] [Google Scholar] · DOI
  23. Chau KY, Munshi N, Keane-Myers A, Cheung-Chau KW, Tai AK, Manfioletti G, Dorey CK, Thanos D, Zack DJ, Ono SJ. The architectural transcription factor high mobility group I(Y) participates in photoreceptor-specific gene expression. J Neurosci. 2000;20:7317–7324. doi: 10.1523/JNEUROSCI.20-19-07317.2000. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  24. Chen F, Figueroa DJ, Marmorstein AD, Zhang Q, Petrukhin K, Caskey CT, Austin CP. Retina-specific nuclear receptor: A potential regulator of cellular retinaldehyde-binding protein expressed in retinal pigment epithelium and Muller glial cells. Proc Natl Acad Sci U S A. 1999;96:15149–15154. doi: 10.1073/pnas.96.26.15149. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  25. Chen J, Rattner A, Nathans J. The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J Neurosci. 2005;25:118–129. doi: 10.1523/JNEUROSCI.3571-04.2005. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  26. Chen J, Rattner A, Nathans J. Effects of L1 retrotransposon insertion on transcript processing, localization and accumulation: lessons from the retinal degeneration 7 mouse and implications for the genomic ecology of L1 elements. Hum Mol Genet. 2006;15:2146–2156. doi: 10.1093/hmg/ddl138. [DOI] [PubMed] [Google Scholar] · DOI
  27. Chen S, Zack DJ. Ret 4, a positive acting rhodopsin regulatory element identified using a bovine retina in vitro transcription system. J Biol Chem. 1996;271:28549–28557. doi: 10.1074/jbc.271.45.28549. [DOI] [PubMed] [Google Scholar] · DOI
  28. Chen S, Wang Q-L, Xu S, Liu Y, Lili YL, Wang Y, Zack DJ. Functional analysis of cone-rod homeobox (CRX) mutations associated with retinal dystrophy. Hum Mol Genet. 2002;11:873–884. doi: 10.1093/hmg/11.8.873. [DOI] [PubMed] [Google Scholar] · DOI
  29. Chen S, Peng GH, Wang X, Smith AC, Grote SK, Sopher BL, La Spada AR. Interference of Crx-dependent transcription by ataxin-7 involves interaction between the glutamine regions and requires the ataxin-7 carboxy-terminal region for nuclear localization. Hum Mol Genet. 2004;13:53–67. doi: 10.1093/hmg/ddh005. [DOI] [PubMed] [Google Scholar] · DOI
  30. Chen S, Wang QL, Nie Z, Sun H, Lennon G, Copeland NG, Gilbert DJ, Jenkins NA, Zack DJ. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron. 1997;19:1017–1030. doi: 10.1016/s0896-6273(00)80394-3. [DOI] [PubMed] [Google Scholar] · DOI
  31. Cheng H, Khanna H, Oh EC, Hicks D, Mitton KP, Swaroop A. Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum Mol Genet. 2004;13:1563–1575. doi: 10.1093/hmg/ddh173. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  32. Cheng H, Aleman TS, Cideciyan AV, Khanna R, Jacobson SG, Swaroop A. In vivo function of the orphan nuclear receptor NR2E3 in establishing photoreceptor identity during mammalian retinal development. Hum Mol Genet. 2006;15:2588–2602. doi: 10.1093/hmg/ddl185. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  33. Chow L, Levine EM, Reh TA. The nuclear receptor transcription factor, retinoid-related orphan receptor beta, regulates retinal progenitor proliferation. Mech Dev. 1998;77:149–164. doi: 10.1016/s0925-4773(98)00135-x. [DOI] [PubMed] [Google Scholar] · DOI
  34. Cissell MA, Zhao L, Sussel L, Henderson E, Stein R. Transcription factor occupancy of the insulin gene in vivo. Evidence for direct regulation by Nkx2.2. J Biol Chem. 2003;278:751–756. doi: 10.1074/jbc.M205905200. [DOI] [PubMed] [Google Scholar] · DOI
  35. Corbo JC, Cepko CL. A hybrid photoreceptor expressing both rod and cone genes in a mouse model of enhanced S-cone syndrome. PLoS Genet. 2005;1:e11. doi: 10.1371/journal.pgen.0010011. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  36. Daniele LL, Lillo C, Lyubarsky AL, Nikonov SS, Philp N, Mears AJ, Swaroop A, Williams DS, Pugh EN., Jr. Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest Ophthalmol Vis Sci. 2005;46:2156–2167. doi: 10.1167/iovs.04-1427. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  37. DeAngelis MM, Grimsby JL, Sandberg MA, Berson EL, Dryja TP. Novel Mutations in the NRL Gene and Associated Clinical Findings in Patients With Dominant Retinitis Pigmentosa. Arch Ophthalmol. 2002;120:369–375. doi: 10.1001/archopht.120.3.369. [DOI] [PubMed] [Google Scholar] · DOI
  38. Diallo EM, Wilhelm KG, Jr., Thompson DL, Koenig RJ. Variable RXR requirements for thyroid hormone responsiveness of endogenous genes. Mol Cell Endocrinol. 2007;264:149–156. doi: 10.1016/j.mce.2006.11.004. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  39. Eckey M, Moehren U, Baniahmad A. Gene silencing by the thyroid hormone receptor. Mol Cell Endocrinol. 2003;213:13–22. doi: 10.1016/j.mce.2003.10.026. [DOI] [PubMed] [Google Scholar] · DOI
  40. Farjo Q, Jackson A, Pieke-Dahl S, Scott K, Kimberling WJ, Sieving PA, Richards JE, Swaroop A. Human bZIP transcription factor gene NRL: structure, genomic sequence, and fine linkage mapping at 14q11.2 and negative mutation analysis in patients with retinal degeneration. Genomics. 1997;45:395–401. doi: 10.1006/geno.1997.4964. [DOI] [PubMed] [Google Scholar] · DOI
  41. Finkelstein R, Boncinelli E. From fly head to mammalian forebrain: the story of otd and Otx. Trends Genet. 1994;10:310–315. doi: 10.1016/0168-9525(94)90033-7. [DOI] [PubMed] [Google Scholar] · DOI
  42. Fong SL, Fong WB. Elements regulating the transcription of human interstitial retinoid- binding protein (IRBP) gene in cultured retinoblastoma cells. Curr Eye Res. 1999;18:283–291. doi: 10.1076/ceyr.18.4.283.5360. [DOI] [PubMed] [Google Scholar] · DOI
  43. Forrest D, Reh TA, Rusch A. Neurodevelopmental control by thyroid hormone receptors. Curr Opin Neurobiol. 2002;12:49–56. doi: 10.1016/s0959-4388(02)00289-1. [DOI] [PubMed] [Google Scholar] · DOI
  44. Freund CL, Wang QL, Chen S, Muskat BL, Wiles CD, Sheffield VC, Jacobson SG, McInnes RR, Zack DJ, Stone EM. De novo mutations in the CRX homeobox gene associated with Leber congenital amaurosis. Nat Genet. 1998;18:311–312. doi: 10.1038/ng0498-311. [DOI] [PubMed] [Google Scholar] · DOI
  45. Freund CL, Gregory-Evans CY, Furukawa T, Papaioannou M, Looser J, Ploder L, Bellingham J, Ng D, Herbrick JA, Duncan A, Scherer SW, Tsui LC, Loutradis-Anagnostou A, Jacobson SG, Cepko CL, Bhattacharya SS, McInnes RR. Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell. 1997;91:543–553. doi: 10.1016/s0092-8674(00)80440-7. [DOI] [PubMed] [Google Scholar] · DOI
  46. Friedman JS, Khanna H, Swain PK, Denicola R, Cheng H, Mitton KP, Weber CH, Hicks D, Swaroop A. The minimal transactivation domain of the basic motif-leucine zipper transcription factor NRL interacts with TATA-binding protein. J Biol Chem. 2004;279:47233–47241. doi: 10.1074/jbc.M408298200. [DOI] [PubMed] [Google Scholar] · DOI
  47. Furukawa A, Koike C, Lippincott P, Cepko CL, Furukawa T. The mouse Crx 5'-upstream transgene sequence directs cell-specific and developmentally regulated expression in retinal photoreceptor cells. J Neurosci. 2002;22:1640–1647. doi: 10.1523/JNEUROSCI.22-05-01640.2002. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  48. Furukawa K. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J Cell Sci. 1999;112:2485–2492. doi: 10.1242/jcs.112.15.2485. [DOI] [PubMed] [Google Scholar] · DOI
  49. Furukawa T, Morrow EM, Cepko CL. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell. 1997;91:531–541. doi: 10.1016/s0092-8674(00)80439-0. [DOI] [PubMed] [Google Scholar] · DOI
  50. Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL. Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet. 1999;23:466–470. doi: 10.1038/70591. [DOI] [PubMed] [Google Scholar] · DOI
  51. Garelli A, Rotstein NP, Politi LE. Docosahexaenoic acid promotes photoreceptor differentiation without altering Crx expression. Invest Ophthalmol Vis Sci. 2006;47:3017–3027. doi: 10.1167/iovs.05-1659. [DOI] [PubMed] [Google Scholar] · DOI
  52. Ghosh JC, Yang X, Zhang A, Lambert MH, Li H, Xu HE, Chen JD. Interactions that determine the assembly of a retinoid X receptor/corepressor complex. Proc Natl Acad Sci U S A. 2002;99:5842–5847. doi: 10.1073/pnas.092043399. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  53. Haider NB, Demarco P, Nystuen AM, Huang X, Smith RS, McCall MA, Naggert JK, Nishina PM. The transcription factor Nr2e3 functions in retinal progenitors to suppress cone cell generation. Vis Neurosci. 2006;23:917–929. doi: 10.1017/S095252380623027X. [DOI] [PubMed] [Google Scholar] · DOI
  54. Haider NB, Jacobson SG, Cideciyan AV, Swiderski R, Streb LM, Searby C, Beck G, Hockey R, Hanna DB, Gorman S, Duhl D, Carmi R, Bennett J, Weleber RG, Fishman GA, Wright AF, Stone EM, Sheffield VC. Mutation of a nuclear receptor gene, NR2E3, causes enhanced S cone syndrome, a disorder of retinal cell fate. Nat Genet. 2000;24:127–131. doi: 10.1038/72777. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  55. Harpavat S, Cepko CL. Thyroid hormone and retinal development: an emerging field. Thyroid. 2003;13:1013–1019. doi: 10.1089/105072503770867183. [DOI] [PubMed] [Google Scholar] · DOI
  56. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet. 2006;368:1795–1809. doi: 10.1016/S0140-6736(06)69740-7. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  57. Haruta M, Kosaka M, Kanegae Y, Saito I, Inoue T, Kageyama R, Nishida A, Honda Y, Takahashi M. Induction of photoreceptor-specific phenotypes in adult mammalian iris tissue. Nat Neurosci. 2001;12:12. doi: 10.1038/nn762. [DOI] [PubMed] [Google Scholar] · DOI
  58. Harvey CB, Bassett JH, Maruvada P, Yen PM, Williams GR. The rat thyroid hormone receptor (TR) {Delta}{beta}3 displays cell-, TR isoform- and thyroid hormone response element specific actions. Endocrinology. 2007 doi: 10.1210/en.2006-1248. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  59. Hatakeyama J, Kageyama R. Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol. 2004;15:83–89. doi: 10.1016/j.semcdb.2003.09.005. [DOI] [PubMed] [Google Scholar] · DOI
  60. Havis E, Le Mevel S, Morvan Dubois G, Shi DL, Scanlan TS, Demeneix BA, Sachs LM. Unliganded thyroid hormone receptor is essential for Xenopus laevis eye development. Embo J. 2006;25:4943–4951. doi: 10.1038/sj.emboj.7601356. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  61. He L, Campbell ML, Srivastava D, Blocker YS, Harris JR, Swaroop A, Fox DA. Spatial and temporal expression of AP-1 responsive rod photoreceptor genes and bZIP transcription factors during development of the rat retina. Mol Vis. 1998;4:32. [PubMed] [Google Scholar]
  62. Hoskins SG. Metamorphosis of the amphibian eye. J Neurobiol. 1990;21:970–989. doi: 10.1002/neu.480210704. [DOI] [PubMed] [Google Scholar] · DOI
  63. Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, Bush RA, Sieving PA, Sheils DM, McNally N, Creighton P, Erven A, Boros A, Gulya K, Capecchi MR, Humphries P. Retinopathy induced in mice by targeted disruption of the rhodopsin gene [see comments]. Nat Genet. 1997;15:216–219. doi: 10.1038/ng0297-216. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  64. Hyatt GA, Dowling JE. Retinoic acid. A key molecule for eye and photoreceptor development. Invest Ophthalmol Vis Sci. 1997;38:1471–1475. [PubMed] [Google Scholar]
  65. Jacobson SG, Sumaroka A, Aleman TS, Cideciyan AV, Schwartz SB, Roman AJ, McInnes RR, Sheffield VC, Stone EM, Swaroop A, Wright AF. Nuclear receptor NR2E3 gene mutations distort human retinal laminar architecture and cause an unusual degeneration. Hum Mol Genet. 2004;13:1893–1902. doi: 10.1093/hmg/ddh198. [DOI] [PubMed] [Google Scholar] · DOI
  66. Janssen JJ, Kuhlmann ED, van Vugt AH, Winkens HJ, Janssen BP, Deutman AF, Driessen CA. Retinoic acid receptors and retinoid X receptors in the mature retina: subtype determination and cellular distribution. Curr Eye Res. 1999;19:338–347. doi: 10.1076/ceyr.19.4.338.5307. [DOI] [PubMed] [Google Scholar] · DOI
  67. Kanda A, Friedman JS, Nishiguchi KM, Swaroop A. Retinopathy mutations in the bZIP protein NRL alter phosphorylation and transcriptional activity. Hum Mutat. 2007;28:589–598. doi: 10.1002/humu.20488. [DOI] [PubMed] [Google Scholar] · DOI
  68. Kobayashi M, Takezawa S, Hara K, Yu RT, Umesono Y, Agata K, Taniwaki M, Yasuda K, Umesono K. Identification of a photoreceptor cell-specific nuclear receptor. Proc Natl Acad Sci U S A. 1999;96:4814–4819. doi: 10.1073/pnas.96.9.4814. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  69. Kumar R, Chen S, Scheurer D, Wang QL, Duh E, Sung CH, Rehemtulla A, Swaroop A, Adler R, Zack DJ. The bZIP transcription factor Nrl stimulates rhodopsin promoter activity in primary retinal cell cultures. J Biol Chem. 1996;271:29612–29618. doi: 10.1074/jbc.271.47.29612. [DOI] [PubMed] [Google Scholar] · DOI
  70. La Spada AR, Fu YH, Sopher BL, Libby RT, Wang X, Li LY, Einum DD, Huang J, Possin DE, Smith AC, Martinez RA, Koszdin KL, Treuting PM, Ware CB, Hurley JB, Ptacek LJ, Chen S. Polyglutamine-expanded ataxin-7 antagonizes CRX function and induces cone-rod dystrophy in a mouse model of SCA7. Neuron. 2001;31:913–927. doi: 10.1016/s0896-6273(01)00422-6. [DOI] [PubMed] [Google Scholar] · DOI
  71. Lerner LE, Gribanova YE, Ji M, Knox BE, Farber DB. Nrl and Sp nuclear proteins mediate transcription of rod-specific cGMP-phosphodiesterase beta-subunit gene: involvement of multiple response elements. J Biol Chem. 2001;276:34999–35007. doi: 10.1074/jbc.M103301200. [DOI] [PubMed] [Google Scholar] · DOI
  72. Li X, Chen S, Wang Q, Zack DJ, Snyder SH, Borjigin J. A pineal regulatory element (PIRE) mediates transactivation by the pineal/retina-specific transcription factor CRX. Proc Natl Acad Sci U S A. 1998;95:1876–1881. doi: 10.1073/pnas.95.4.1876. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  73. Liu Q, Ji X, Breitman ML, Hitchcock PF, Swaroop A. Expression of the bZIP transcription factor gene Nrl in the developing nervous system. Oncogene. 1996;12:207–211. [PubMed] [Google Scholar]
  74. Lukats A, Szabo A, Rohlich P, Vigh B, Szel A. Photopigment coexpression in mammals: comparative and developmental aspects. Histol Histopathol. 2005;20:551–574. doi: 10.14670/HH-20.551. [DOI] [PubMed] [Google Scholar] · DOI
  75. Luo T, Sakai Y, Wagner E, Drager UC. Retinoids, eye development, and maturation of visual function. J Neurobiol. 2006;66:677–686. doi: 10.1002/neu.20239. [DOI] [PubMed] [Google Scholar] · DOI
  76. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR. Retinal repair by transplantation of photoreceptor precursors. Nature. 2006;444:203–207. doi: 10.1038/nature05161. [DOI] [PubMed] [Google Scholar] · DOI
  77. Makowski A, Brzostek S, Cohen RN, Hollenberg AN. Determination of nuclear receptor corepressor interactions with the thyroid hormone receptor. Mol Endocrinol. 2003;17:273–286. doi: 10.1210/me.2002-0310. [DOI] [PubMed] [Google Scholar] · DOI
  78. Mali RS, Zhang X, Hoerauf W, Doyle D, Devitt J, Loffreda-Wren J, Mitton KP. FIZ1 is expressed during photoreceptor maturation, and synergizes with NRL and CRX at rod-specific promoters in vitro. Exp Eye Res. 2007;84:349–360. doi: 10.1016/j.exer.2006.10.009. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  79. Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell. 1995;83:841–850. doi: 10.1016/0092-8674(95)90200-7. [DOI] [PubMed] [Google Scholar] · DOI
  80. Martinez E, Palhan VB, Tjernberg A, Lymar ES, Gamper AM, Kundu TK, Chait BT, Roeder RG. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol Cell Biol. 2001;21:6782–6795. doi: 10.1128/MCB.21.20.6782-6795.2001. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  81. Martinez-Gimeno M, Maseras M, Baiget M, Beneito M, Antinolo G, Ayuso C, Carballo M. Mutations P51U and G122E in retinal transcription factor NRL associated with autosomal dominant and sporadic retinitis pigmentosa. Hum Mutat. 2001;17:520. doi: 10.1002/humu.1135. [DOI] [PubMed] [Google Scholar] · DOI
  82. Martinez-Morales JR, Signore M, Acampora D, Simeone A, Bovolenta P. Otx genes are required for tissue specification in the developing eye. Development. 2001;128:2019–2030. doi: 10.1242/dev.128.11.2019. [DOI] [PubMed] [Google Scholar] · DOI
  83. Martinez-Morales JR, Dolez V, Rodrigo I, Zaccarini R, Leconte L, Bovolenta P, Saule S. OTX2 activates the molecular network underlying retina pigment epithelium differentiation. J Biol Chem. 2003;278:21721–21731. doi: 10.1074/jbc.M301708200. [DOI] [PubMed] [Google Scholar] · DOI
  84. Matsuo I, Kuratani S, Kimura C, Takeda N, Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 1995;9:2646–2658. doi: 10.1101/gad.9.21.2646. [DOI] [PubMed] [Google Scholar] · DOI
  85. Milam AH, Rose L, Cideciyan AV, Barakat MR, Tang WX, Gupta N, Aleman TS, Wright AF, Stone EM, Sheffield VC, Jacobson SG. The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration. Proc Natl Acad Sci U S A. 2002;99:473–478. doi: 10.1073/pnas.022533099. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  86. Mitton KP, Swain PK, Chen S, Xu S, Zack DJ, Swaroop A. The leucine zipper of NRL interacts with the CRX homeodomain. A possible mechanism of transcriptional synergy in rhodopsin regulation. J Biol Chem. 2000;275:29794–29799. doi: 10.1074/jbc.M003658200. [DOI] [PubMed] [Google Scholar] · DOI
  87. Mitton KP, Swain PK, Khanna H, Dowd M, Apel IJ, Swaroop A. Interaction of retinal bZIP transcription factor NRL with Flt3-interacting zinc-finger protein Fiz1: possible role of Fiz1 as a transcriptional repressor. Hum Mol Genet. 2003;12:365–373. doi: 10.1093/hmg/ddg035. [DOI] [PubMed] [Google Scholar] · DOI
  88. Mori M, Ghyselinck NB, Chambon P, Mark M. Systematic immunolocalization of retinoid receptors in developing and adult mouse eyes. Invest Ophthalmol Vis Sci. 2001;42:1312–1318. [PubMed] [Google Scholar]
  89. Morrow EM, Furukawa T, Lee JE, Cepko CL. NeuroD regulates multiple functions in the developing neural retina in rodent. Development. 1999;126:23–36. doi: 10.1242/dev.126.1.23. [DOI] [PubMed] [Google Scholar] · DOI
  90. Ng L, Hurley JB, Dierks B, Srinivas M, Salto C, Vennstrom B, Reh TA, Forrest D. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet. 2001;27:94–98. doi: 10.1038/83829. [DOI] [PubMed] [Google Scholar] · DOI
  91. Nikonov SS, Kholodenko R, Lem J, Pugh EN., Jr. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J Gen Physiol. 2006;127:359–374. doi: 10.1085/jgp.200609490. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  92. Nikonov SS, Daniele LL, Zhu X, Craft CM, Swaroop A, Pugh EN., Jr. Photoreceptors of Nrl −/− mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms. J Gen Physiol. 2005;125:287–304. doi: 10.1085/jgp.200409208. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  93. Nishida A. [Mechanisms of retinal photoreceptor cell fate determination]. Nippon Ganka Gakkai Zasshi. 2005;109:708–716. [PubMed] [Google Scholar]
  94. Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, Matsuo I, Furukawa T. Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci. 2003;6:1255–1263. doi: 10.1038/nn1155. [DOI] [PubMed] [Google Scholar] · DOI
  95. Nishiguchi KM, Friedman JS, Sandberg MA, Swaroop A, Berson EL, Dryja TP. Recessive NRL mutations in patients with clumped pigmentary retinal degeneration and relative preservation of blue cone function. Proc Natl Acad Sci U S A. 2004;101:17819–17824. doi: 10.1073/pnas.0408183101. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  96. Oh EC, Khan N, Novelli E, Khanna H, Strettoi E, Swaroop A. From the Cover: Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc Natl Acad Sci U S A. 2007;104:1679–1684. doi: 10.1073/pnas.0605934104. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  97. Olsson JE, Gordon JW, Pawlyk BS, Roof D, Hayes A, Molday RS, Mukai S, Cowley GS, Berson EL, Dryja TP. Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron. 1992;9:815–830. doi: 10.1016/0896-6273(92)90236-7. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  98. Palhan VB, Chen S, Peng GH, Tjernberg A, Gamper AM, Fan Y, Chait BT, La Spada AR, Roeder RG. Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc Natl Acad Sci U S A. 2005;102:8472–8477. doi: 10.1073/pnas.0503505102. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  99. Peichl L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol. 2005;287:1001–1012. doi: 10.1002/ar.a.20262. [DOI] [PubMed] [Google Scholar] · DOI
  100. Peng GH, Chen S. Chromatin immunoprecipitation identifies photoreceptor transcription factor targets in mouse models of retinal degeneration: new findings and challenges. Vis Neurosci. 2005;22:575–586. doi: 10.1017/S0952523805225063. [DOI] [PubMed] [Google Scholar] · DOI
  101. Peng GH, Ahmad O, Ahmad F, Liu J, Chen S. The photoreceptor-specific nuclear receptor Nr2e3 interacts with Crx and exerts opposing effects on the transcription of rod versus cone genes. Hum Mol Genet. 2005;14:747–764. doi: 10.1093/hmg/ddi070. [DOI] [PubMed] [Google Scholar] · DOI
  102. Pennesi ME, Cho JH, Yang Z, Wu SH, Zhang J, Wu SM, Tsai MJ. BETA2/NeuroD1 null mice: a new model for transcription factor-dependent photoreceptor degeneration. J Neurosci. 2003;23:453–461. doi: 10.1523/JNEUROSCI.23-02-00453.2003. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  103. Plouhinec JL, Sauka-Spengler T, Germot A, Le Mentec C, Cabana T, Harrison G, Pieau C, Sire JY, Veron G, Mazan S. The mammalian Crx genes are highly divergent representatives of the Otx5 gene family, a gnathostome orthology class of orthodenticle-related homeogenes involved in the differentiation of retinal photoreceptors and circadian entrainment. Mol Biol Evol. 2003;20:513–521. doi: 10.1093/molbev/msg085. [DOI] [PubMed] [Google Scholar] · DOI
  104. Ragge NK, Brown AG, Poloschek CM, Lorenz B, Henderson RA, Clarke MP, Russell-Eggitt I, Fielder A, Gerrelli D, Martinez-Barbera JP, Ruddle P, Hurst J, Collin JR, Salt A, Cooper ST, Thompson PJ, Sisodiya SM, Williamson KA, Fitzpatrick DR, van Heyningen V, Hanson IM. Heterozygous mutations of OTX2 cause severe ocular malformations. Am J Hum Genet. 2005;76:1008–1022. doi: 10.1086/430721. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  105. Rehemtulla A, Warwar R, Kumar R, Ji X, Zack DJ, Swaroop A. The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc Natl Acad Sci U S A. 1996;93:191–195. doi: 10.1073/pnas.93.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  106. Rivolta C, Berson EL, Dryja TP. Dominant Leber congenital amaurosis, cone-rod degeneration, and retinitis pigmentosa caused by mutant versions of the transcription factor CRX. Hum Mutat. 2001a;18:488–498. doi: 10.1002/humu.1226. [DOI] [PubMed] [Google Scholar] · DOI
  107. Rivolta C, Peck NE, Fulton AB, Fishman GA, Berson EL, Dryja TP. Novel frameshift mutations in CRX associated with Leber congenital amaurosis. Hum Mutat. 2001b;18:550–551. doi: 10.1002/humu.1243. [DOI] [PubMed] [Google Scholar] · DOI
  108. Roberts MR, Hendrickson A, McGuire CR, Reh TA. Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest Ophthalmol Vis Sci. 2005;46:2897–2904. doi: 10.1167/iovs.05-0093. [DOI] [PubMed] [Google Scholar] · DOI
  109. Roberts MR, Srinivas M, Forrest D, Morreale de Escobar G, Reh TA. Making the gradient: thyroid hormone regulates cone opsin expression in the developing mouse retina. Proc Natl Acad Sci U S A. 2006;103:6218–6223. doi: 10.1073/pnas.0509981103. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  110. Rodieck RW. The First Steps in Seeing. 1 Edition. Sinauer Associates, Inc.; Sunderland, MA: 1998. [Google Scholar]
  111. Rohlich P, van Veen T, Szel A. Two different visual pigments in one retinal cone cell. Neuron. 1994;13:1159–1166. doi: 10.1016/0896-6273(94)90053-1. [DOI] [PubMed] [Google Scholar] · DOI
  112. Scheetz TE, Kim KY, Swiderski RE, Philp AR, Braun TA, Knudtson KL, Dorrance AM, DiBona GF, Huang J, Casavant TL, Sheffield VC, Stone EM. Regulation of gene expression in the mammalian eye and its relevance to eye disease. Proc Natl Acad Sci U S A. 2006;103:14429–14434. doi: 10.1073/pnas.0602562103. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  113. Shibusawa N, Hashimoto K, Nikrodhanond AA, Liberman MC, Applebury ML, Liao XH, Robbins JT, Refetoff S, Cohen RN, Wondisford FE. Thyroid hormone action in the absence of thyroid hormone receptor DNA-binding in vivo. J Clin Invest. 2003;112:588–597. doi: 10.1172/JCI18377. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  114. Sohocki MM, Sullivan LS, Mintz-Hittner HA, Birch D, Heckenlively JR, Freund CL, McInnes RR, Daiger SP. A range of clinical phenotypes associated with mutations in CRX, a photoreceptor transcription-factor gene. Am J Hum Genet. 1998;63:1307–1315. doi: 10.1086/302101. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  115. Srinivas M, Ng L, Liu H, Jia L, Forrest D. Activation of the blue opsin gene in cone photoreceptor development by retinoid-related orphan receptor beta. Mol Endocrinol. 2006;20:1728–1741. doi: 10.1210/me.2005-0505. [DOI] [PubMed] [Google Scholar] · DOI
  116. Strettoi E, Mears AJ, Swaroop A. Recruitment of the rod pathway by cones in the absence of rods. J Neurosci. 2004;24:7576–7582. doi: 10.1523/JNEUROSCI.2245-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  117. Swain PK, Hicks D, Mears AJ, Apel IJ, Smith JE, John SK, Hendrickson A, Milam AH, Swaroop A. Multiple phosphorylated isoforms of NRL are expressed in rod photoreceptors. J Biol Chem. 2001;276:36824–36830. doi: 10.1074/jbc.M105855200. [DOI] [PubMed] [Google Scholar] · DOI
  118. Swaroop A, Xu I, Pawar H, Jackson A, Skolnick C. A conserved retina-specific gene encodes a basic motif/leuctre zipper domain. Proc Natl Acad Sci U S A. 1992;89:266–270. doi: 10.1073/pnas.89.1.266. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  119. Szanto A, Narkar V, Shen Q, Uray IP, Davies PJ, Nagy L. Retinoid X receptors: X-ploring their (patho)physiological functions. Cell Death Differ 11 Suppl. 2004;2:S126–143. doi: 10.1038/sj.cdd.4401533. [DOI] [PubMed] [Google Scholar] · DOI
  120. Tahayato A, Sonneville R, Pichaud F, Wernet MF, Papatsenko D, Beaufils P, Cook T, Desplan C. Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev Cell. 2003;5:391–402. doi: 10.1016/s1534-5807(03)00239-9. [DOI] [PubMed] [Google Scholar] · DOI
  121. Takezawa S, Yokoyama A, Okada M, Fujiki R, Iriyama A, Yanagi Y, Ito H, Takada I, Kishimoto M, Miyajima A, Takeyama KI, Umesono K, Kitagawa H, Kato S. A cell cycle-dependent co-repressor mediates photoreceptor cell-specific nuclear receptor function. Embo J. 2007 doi: 10.1038/sj.emboj.7601548. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted] · DOI
  122. Treisman J, Gonczy P, Vashishtha M, Harris E, Desplan C. A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell. 1989;59:553–562. doi: 10.1016/0092-8674(89)90038-x. [DOI] [PubMed] [Google Scholar] · DOI
  123. Turner DL, Cepko CL. A common progenitor for neurons and glia persists in rat retina late in development. Nature. 1987;328:131–136. doi: 10.1038/328131a0. [DOI] [PubMed] [Google Scholar] · DOI
  124. Ueno S, Kondo M, Miyata K, Hirai T, Miyata T, Usukura J, Nishizawa Y, Miyake Y. Physiological function of S-cone system is not enhanced in rd7 mice. Exp Eye Res. 2005;81:751–758. doi: 10.1016/j.exer.2005.04.013. [DOI] [PubMed] [Google Scholar] · DOI
  125. Vandendries ER, Johnson D, Reinke R. orthodenticle is required for photoreceptor cell development in the Drosophila eye. Dev Biol. 1996;173:243–255. doi: 10.1006/dbio.1996.0020. [DOI] [PubMed] [Google Scholar] · DOI
  126. von Schantz M, Lucas RJ, Foster RG. Circadian oscillation of photopigment transcript levels in the mouse retina. Brain Res Mol Brain Res. 1999;72:108–114. doi: 10.1016/s0169-328x(99)00209-0. [DOI] [PubMed] [Google Scholar] · DOI
  127. Wang QL, Chen S, Esumi N, Swain PK, Haines HS, Peng G, Melia BM, McIntosh I, Heckenlively JR, Jacobson SG, Stone EM, Swaroop A, Zack DJ. QRX, a novel homeobox gene, modulates photoreceptor gene expression. Hum Mol Genet. 2004;13:1025–1040. doi: 10.1093/hmg/ddh117. [DOI] [PubMed] [Google Scholar] · DOI
  128. Wang X, Xu S, Rivolta C, Li LY, Peng GH, Swain PK, Sung CH, Swaroop A, Berson EL, Dryja TP, Chen S. Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J Biol Chem. 2002;277:43288–43300. doi: 10.1074/jbc.M207952200. [DOI] [PubMed] [Google Scholar] · DOI
  129. Watanabe T, Raff MC. Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron. 1990;4:461–467. doi: 10.1016/0896-6273(90)90058-n. [DOI] [PubMed] [Google Scholar] · DOI
  130. Wetts R, Fraser SE. Multipotent precursors can give rise to all major cell types of the frog retina. Science. 1988;239:1142–1145. doi: 10.1126/science.2449732. [DOI] [PubMed] [Google Scholar] · DOI
  131. Wright AF, Reddick AC, Schwartz SB, Ferguson JS, Aleman TS, Kellner U, Jurklies B, Schuster A, Zrenner E, Wissinger B, Lennon A, Shu X, Cideciyan AV, Stone EM, Jacobson SG, Swaroop A. Mutation analysis of NR2E3 and NRL genes in Enhanced S Cone Syndrome. Hum Mutat. 2004;24:439. doi: 10.1002/humu.9285. [DOI] [PubMed] [Google Scholar] · DOI
  132. Yan RT, Ma W, Liang L, Wang SZ. bHLH genes and retinal cell fate specification. Mol Neurobiol. 2005;32:157–171. doi: 10.1385/MN:32:2:157. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  133. Yanagi Y, Takezawa S, Kato S. Distinct functions of photoreceptor cell-specific nuclear receptor, thyroid hormone receptor beta2 and CRX in one photoreceptor development. Invest Ophthalmol Vis Sci. 2002;43:3489–3494. [PubMed] [Google Scholar]
  134. Yanagi Y, Masuhiro Y, Mori M, Yanagisawa J, Kato S. p300/CBP acts as a coactivator of the cone-rod homeobox transcription factor. Biochem Biophys Res Commun. 2000;269:410–414. doi: 10.1006/bbrc.2000.2304. [DOI] [PubMed] [Google Scholar] · DOI
  135. Yen PM, Sunday ME, Darling DS, Chin WW. Isoform-specific thyroid hormone receptor antibodies detect multiple thyroid hormone receptors in rat and human pituitaries. Endocrinology. 1992;130:1539–1546. doi: 10.1210/endo.130.3.1537303. [DOI] [PubMed] [Google Scholar] · DOI
  136. Yin L, Wang J, Klein PS, Lazar MA. Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock. Science. 2006;311:1002–1005. doi: 10.1126/science.1121613. [DOI] [PubMed] [Google Scholar] · DOI
  137. Yoshida S, Mears AJ, Friedman JS, Carter T, He S, Oh E, Jing Y, Farjo R, Fleury G, Barlow C, Hero AO, Swaroop A. Expression profiling of the developing and mature Nrl−/− mouse retina: identification of retinal disease candidates and transcriptional regulatory targets of Nrl. Hum Mol Genet. 2004;13:1487–1503. doi: 10.1093/hmg/ddh160. [DOI] [PubMed] [Google Scholar] · DOI
  138. Young RW. Cell differentiation in the retina of the mouse. Anat Rec. 1985;212:199–205. doi: 10.1002/ar.1092120215. [DOI] [PubMed] [Google Scholar] · DOI
  139. Yu J, He S, Friedman JS, Akimoto M, Ghosh D, Mears AJ, Hicks D, Swaroop A. Altered Expression of Genes of the Bmp/Smad and Wnt/Calcium Signaling Pathways in the Cone-only Nrl−/− Mouse Retina, Revealed by Gene Profiling Using Custom cDNA Microarrays. J Biol Chem. 2004;279:42211–42220. doi: 10.1074/jbc.M408223200. [DOI] [PubMed] [Google Scholar] · DOI
  140. Yu X, Lin J, Zack DJ, Qian J. Computational analysis of tissue-specific combinatorial gene regulation: predicting interaction between transcription factors in human tissues. Nucleic Acids Res. 2006;34:4925–4936. doi: 10.1093/nar/gkl595. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  141. Zhang CL, Zou Y, Yu RT, Gage FH, Evans RM. Nuclear receptor TLX prevents retinal dystrophy and recruits the corepressor atrophin1. Genes Dev. 2006;20:1308–1320. doi: 10.1101/gad.1413606. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI

Authors
Hennig, A. K., Peng, G.-H., & Chen, S.
Affiliations
Washington University in St. Louis (US)
Corresponding author
Chen, Shiming
ORCID
Venue
Brain Research
Publisher
Elsevier BV
Published
2008-02
Volume
1192
Pages
114-133
ISSN
0006-8993 (ISSN-L)
DOI
10.1016/j.brainres.2007.06.036
PMC
PMC2266892
OpenAlex
W2049890303
Cited by
214
References
158
Citations by year
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FWCI
4.76
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Eye Institute (EY12543, EY 02687, P30EY002687, R01EY012543)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
Keywords
photoreceptor development, rod photoreceptors, cone photoreceptors, CRX, transcriptional regulatory networks, NRL, NR2E3, retinoid X receptor gamma, transcriptional regulation, photoreceptor degeneration
MeSH terms
Animals, Cell Differentiation, Humans, Photoreceptor Cells, Receptors, Cell Surface, Retinal Diseases, Stem Cells, Transcription Factors, Signal Transduction, Trans-Activators, Homeodomain Proteins, Gene Expression Regulation, Developmental, Feedback, Physiological

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