Nr2e3-directed transcriptional regulation of genes involved in photoreceptor development and cell-type specific phototransduction

Experimental Eye Research

Volumn 89, Issue 3, 2009, Pages 365-372

  Haider, Neena B ^a,b   Mollema, Nissa ^a   Gaule, Meghan ^a   Yuan, Yang ^a   Sachs, Andrew J ^a   Nystuen, Arne M ^a   Naggert, Jürgen K ^c   Nishina, Patsy M ^c  

^a NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

development; Enhanced S cone syndrome; gene expression; Nr2e3; phototransduction; rd7; retina; retinitis pigmentosa

Indexed keywords

ALPHA CRYSTALLIN; BIOLOGICAL FACTOR; GAMMA B CRYSTALLIN; GAMMA CRYSTALLIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA TRANSDUCING 2; GUANINE NUCLEOTIDE BINDING PROTEIN BETA 1; GUANINE NUCLEOTIDE BINDING PROTEIN BETA POLYPEPTIDE 3; GUANYLATE CYCLASE ACTIVATOR; GUANYLATE CYCLASE ACTIVATOR 1A; INTERPHOTORECEPTOR RETINOID BINDING PROTEIN; NUCLEAR PROTEIN; NUCLEAR PROTEIN 1; OPSIN; RECOVERIN; RHODOPSIN; RHODOPSIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NUCLEAR RECEPTOR SUB FAMILY 1 GROUP C MEMBER 1; TRANSCRIPTION FACTOR NUCLEAR RECEPTOR SUB FAMILY 1 GROUP D MEMBER 1; TRANSCRIPTION FACTOR NUCLEAR RECEPTOR SUB FAMILY 2 GROUP E MEMBER 3; TRANSCRIPTION FACTOR NUCLEAR RECEPTOR SUB FAMILY 2 GROUP E MEMBER 3 RETINAL DEGENERATION 7 RETINAL DEGENARATION 7; TRANSCRIPTION FACTOR RAR RELATED ORPHAN RECEPTOR ALPHA; TRANSCRIPTION FACTOR RAR RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 1; TRANSDUCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; MOUSE; MUTANT; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RETINA CONE; RETINA DEVELOPMENT; RETINA ROD; SUBTRACTIVE HYBRIDIZATION; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; DISEASE MODELS, ANIMAL; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIGHT SIGNAL TRANSDUCTION; MICE; MICE, MUTANT STRAINS; PHOTORECEPTOR CELLS, VERTEBRATE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RETINA; RETINAL DEGENERATION; TRANSCRIPTION FACTORS;

EID: 67651213785     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2009.04.006     Document Type: Article

References (37)

1. Akhmedov N.B., Piriev N.I., Chang B., Rappoport A.L., Hawes N.L., Nishina P.M., Nusinowitz S., Heckenlively J.R., Roderick T.H., Kozak C.A., Danciger M., Davisson M.T., and Farber D.B. A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in rd7 mouse. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 5551-5556
2. Chavala S.H., Sari A., Lewis H., Pauer G.J., Simpson E., Hagstrom S.A., and Traboulsi E.I. An Arg311Gln NR2E3 mutation in a family with classic Goldmann-Favre syndrome. Br. J. Ophthalmol. 89 (2005) 1065-1066
3. Chen J., Rattner A., and Nathans J. The rod photoreceptor-specific nuclear receptor Nr2e3 suppresses transcription of multiple cone-specific genes. J. Neurosci. 25 (2005) 118-129
4. Cheng H., Khanna H., Oh E.C., Hicks D., Mitton K.P., and Swaroop A. Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum. Mol. Genet. 13 (2004) 1563-1575
5. Cheng H., Aleman T.S., Cideciyan A.V., Khanna R., Jacobson S.G., and Swaroop A. In vivo function of the orphan nuclear receptor NR2E3 in establishing photoreceptor identity during mammalian retinal development. Hum. Mol. Genet. 15 (2006) 2588-2602
6. Coppieters F., Leroy B.P., Beysen D., Hellemans J., De Bosscher K., Haegeman G., Robberecht K., Wuyts W., Coucke P.J., and De Baere E. Recurrent mutation in the first zinc finger of the orphan nuclear receptor NR2E3 causes autosomal dominant retinitis pigmentosa. Am. J. Hum. Genet. 81 (2007) 147-157
7. Corbo J.C., and Cepko C.L. A hybrid photoreceptor expressing both rod and cone genes in a mouse model of enhanced S-cone syndrome. PLoS Genet. 5 (2005) 140-153
8. Favre M.A. A propos de deux cas de degenerescence hyaloideoretinienne. Ophthalmologica 135 (1958) 604-609
9. Fishman G.A., Jampol L.M., and Goldberg M.F. Diagnostic features of the Favre-Goldmann syndrome. Br. J. Ophthalmol. 60 (1976) 345-353
10. Gerber S., Rozet J.M., Takezawa S.I., dos Santos L.C., Lopes L., Gribouval O., Penet C., Perrault I., Ducroq D., Souied E., Jeanpierre M., Romana S., Frézal J., Ferraz F., Yu-Umesono R., Munnich A., and Kaplan J. The photoreceptor cell-specific nuclear receptor gene (PNR) accounts for retinitis pigmentosa in the Crypto-Jews from Portugal (Marranos), survivors from the Spanish Inquisition. Hum. Genet. 107 (2000) 276-284
11. Gire A.I., Sullivan L.S., Bowne S.J., Birch D.G., Hughbanks-Wheaton D., Heckenlively J.R., and Daiger S.P. The Gly56Arg mutation in NR2E3 accounts for 1-2% of autosomal dominant retinitis pigmentosa. Mol. Vis. 13 (2007) 1970-1975
12. Haider N.B., Jacobson S.G., Cideciyan A.V., Swideski R., Streb L.M., Searby C., Beck G., Hockey R., Hanna D.B., Gorman S., Duhl D., Carmi R., Bennett J., Weleber R.G., Fishman G.A., Wright A.F., Stone E.M., and Sheffield V.C. Mutation of a nuclear receptor gene, NR2E3, causes enhanced s cone syndrome, a disorder of retinal cell fate. Nat. Genet. 24 (2000) 127-131
13. Haider N.B., Naggert J.K., and Nishina P.M. Excess cone cell proliferation due to lack of a functional NR2E3 causes retinal dysplasia and degeneration in rd7/rd7 mice. Hum. Mol. Genet. 10 (2001) 1619-1626
14. Haider N.B., DeMarco P., Huang X., Nystuen A., Smith R.S., McCall M.A., Naggert J.K., and Nishina P.M. The transcription factor, Nr2e3, functions in retinal progenitors to suppresses cone cell generation. Vis. Neurosci. 23 (2006) 917-929
15. Hawes N.L., Smith R.S., Chang B., Davisson M., Heckenlively J.R., and John S.W. Mouse fundus photography and angiography: a catalogue of normal and mutant phenotypes. Mol. Vis. 5 (1999) 22
16. Hayashi T., Gekka T., Goto-Omoto S., Takeuchi T., Kubo A., and Kitahara K. Novel NR2E3 mutations (R104Q, R334G) associated with a mild form of enhanced S-cone syndrome demonstrate compound heterozygosity. Ophthalmology 112 (2005) 2115
17. Hennig A.K., Peng G.H., and Chen S. Regulation of photoreceptor gene expression by Crx-associated transcription factor network. Brain Res. 1192 (2008) 114-133
18. Jacobson S.G., Marmor M.F., Kemp C.M., and Knighton R.W. SWS (blue) cone hypersensitivity in a newly identified retinal degeneration. Invest. Ophthalmol. Vis. Sci. 31 (1990) 827-838
19. Jacobson S.G., Roman A.J., Roman M.I., Gass J.D.M., and Parker J.A. Relatively enhanced S cone function in the Goldmann-Favre Syndrome. Am. J. Ophthalmol. 111 (1991) 446-453
20. Jacobson S.G., Sumaroka A.l., Aleman T.S., Cideciyan A.V., Schwartz S.B., Roman A.J., McInnes R.R., Sheffield V.C., Stone E.M., Swaroop A., and Wright A.F. Nuclear receptor NR2E3 gene mutations distort human retinal laminar architecture and cause an unusual degeneration. Hum. Mol. Genet. 13 (2004) 1893-1902
21. Kapitskaya M., Cunningham M.E., Lacson R., Kornienko O., Bednar B., and Petrukhin K. Development of the high throughput screening assay for identification of agonists of an orphan nuclear receptor. Assay Drug Dev. Technol. 4 (2006) 253-262
22. Kobayashi M., Takezawa S., Hara K., Yu R.T., Umesono Y., Agata K., Taniwaki M., Yasuda K., and Umesono K. Identification of a photoreceptor cell-specific nuclear receptor. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 4814-4819
23. Lam B.L., Goldberg J.L., Hartley K.L., Stone E.M., and Liu M. Atypical mild enhanced S-cone syndrome with novel compound heterozygosity of the NR2E3 gene. Am. J. Ophthalmol. 144 (2007) 157-159
24. Marmor M.F., Jacobson S.G., Foerster M.H., Kellner U., and Weleber R.G. Diagnostic clinical findings of a new syndrome with night blindness, maculopathy, and enhanced S cone sensitivity. Am. J. Ophthalmol. 110 (1990) 124-134
25. McIlvain V.A., and Knox B.E. Nr2e3 and Nrl can reprogram retinal precursors to the rod fate in Xenopus retina. Dev. Dyn. 236 (2007) 1970-1979
26. Milam A.H., Rose L., Cideciyan A.V., Barakat M.R., Tang W.X., Gupta N., Aleman T.S., Wright A.F., Stone E.M., Sheffield V.C., and Jacobson S.G. The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 473-478
27. Nakamura Y., Hayashi T., Kozaki K., Kubo A., Omoto S., Watanabe A., Toda K., Takeuchi T., Gekka T., and Kitahara K. Enhanced S-cone syndrome in a Japanese family with a nonsense NR2E3 mutation (Q350X). Acta Ophthalmol. Scand. 82 (2004) 616-622
28. Nystuen A.M., Sachs A.J., Yuan Y., Heuermann L., and Haider N.B. A novel mutation in Prph2, a gene regulated by Nr2e3, causes retinal degeneration and outer-segment defects similar to Nr2e3 (rd7/rd7) retinas. Mamm Genome 19 (2008) 623-633
29. Oh E.C., Cheng H., Hao H., Jia L., Khan N.W., and Swaroop A. Rod differentiation factor NRL activates the expression of nuclear receptor NR2E3 to suppress the development of cone photoreceptors. Brain Res. 1236 (2008) 16-29
30. Peng G.H., Ahmad O., Ahmad F., Liu J., and 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. 14 (2005) 747-764
31. Sharon D., Sandberg M.A., Caruso R.C., Berson E.L., and Dryja T.P. Shared mutations in NR2E3 in enhanced S-cone syndrome, Goldmann-Favre syndrome, and many cases of clumped pigmentary retinal degeneration. Arch. Ophthalmol. 121 (2003) 1316-1323
32. Sun G., Yu R.T., Evans R.M., and Shi Y. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 15282-15287
33. Takezawa S., Yokoyama A., Okada M., Fujiki R., Iriyama A., Yanagi Y., Ito H., Takada I., Kishimoto M., Miyajima A., Takeyama K., Umesono K., Kitagawa H., and Kato S. A cell cycle-dependent co-repressor mediates photoreceptor cell-specific nuclear receptor function. EMBO J. 26 (2007) 764-774
34. Webber A.L., Hodor P., Thut C.J., Vogt T.F., Zhang T., Holder D.J., and Petrukhin K. Dual role of Nr2e3 in photoreceptor development and maintenance. Exp. Eye Res. 87 (2008) 35-48
35. Wokennberg S.E., Zhao Z., Kapitskaya M., Webber A.L., Petrukhin K., Tang Y.S., Dean D.C., Hartman G.D., and Lindsley C.W. Identification of potent agonists of photoreceptor-specific nuclear receptor (NR2E3) and preparation of a radioligand. Bioorg. Med. Chem. Lett. 16 (2006) 5001-5004
36. Yanagi Y., Takezawa S., and Kato S. Distinct functions of photoreceptor cell-specific nuclear receptor, thyroid hormone receptor beta2 and CRX in one photoreceptor development. Invest. Ophthalmol. Vis. Sci. 43 (2002) 3489-3494
37. Zhang C.L., Zou Y., Yu R.T., Gage F.H., and Evans R.M. Nuclear receptor TLX prevents retinal dystrophy and recruits the corepressor atrophin1. Genes Dev. 20 (2006) 1308-1320