Dual role of Nr2e3 in photoreceptor development and maintenance

Experimental Eye Research

Volumn 87, Issue 1, 2008, Pages 35-48

  Webber, Andrea L ^a   Hodor, Paul ^a   Thut, Catherine J ^a   Vogt, Thomas F ^a   Zhang, Theresa ^a   Holder, Daniel J ^a   Petrukhin, Konstantin ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

expression profiling; microarray; Nr2e3; nuclear receptor; photoreceptor; rd7; retinal degeneration

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NR2E3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; GENE; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOCUS; MOUSE; NONHUMAN; NR2E3 GENE; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEVELOPMENT;

ANIMALS; EYE PROTEINS; FEMALE; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PHOTORECEPTOR CELLS, VERTEBRATE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RETINA;

EID: 46249085711     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2008.04.006     Document Type: Article

References (53)

1. Akhmedov N.B., Piriev N.I., Chang B., Rapoport 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 the rd7 mouse. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 5551-5556
2. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., and Sherlock G. Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25 (2000) 25-29
3. Bairoch A., Boeckmann B., Ferro S., and Gasteiger E. Swiss-Prot: juggling between evolution and stability. Brief Bioinform. 5 (2004) 39-55
4. Bumsted O'Brien K.M., Cheng H., Jiang Y., Schulte D., Swaroop A., and Hendrickson A.E. Expression of photoreceptor-specific nuclear receptor NR2E3 in rod photoreceptors of fetal human retina. Invest. Ophthalmol. Vis. Sci. 45 (2004) 2807-2812
5. Cepko C.L. The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr. Opin. Neurobiol. 9 (1999) 37-46
6. 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
7. Chen F., Figueroa D.J., Marmorstein A.D., Zhang Q., Petrukhin K., Caskey C.T., and Austin C.P. Retina-specific nuclear receptor: a potential regulator of cellular retinaldehyde-binding protein expressed in retinal pigment epithelium and Müller glial cells. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 15149-15154
8. Chen J., Rattner A., and Nathans J. The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J. Neurosci. 25 (2005) 118-129
9. 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
10. 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
11. Conley Y.P., Thalamuthu A., Jakobsdottir J., Weeks D.E., Mah T., Ferrell R.E., and Gorin M.B. Candidate gene analysis suggests a role for fatty acid biosynthesis and regulation of the complement system in the etiology of age-related maculopathy. Hum. Mol. Genet. 14 (2005) 1991-2002
12. 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. 1 (2005) 0140-0153
13. Edwards A.O., Ritter R., Abel K.J., Manning A., Panhuysen C., and Farrer L.A. Complement factor H polymorphism and age-related macular degeneration. Science 308 (2005) 421-424
14. 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., Frezal 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
15. Gold B., Merriam J.E., Zernant J., Hancox L.S., Taiber A.J., Gehrs K., Cramer K., Neel J., Bergeron J., Barile G.R., Smith R.T., Hageman G.S., Dean M., Allikmets R., and AMD Genetics Clinical Study Group. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat. Genet. 38 (2006) 458-462
16. Gould D.B., Libby R.T., Phalan C., Smith R.S., and John S.W.M. Mice with a Col4a1 mutation have phenotypes relevant to human age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 47 (2006) (E-Abstract 5914)
17. Hackam A.S. The Wnt signaling pathway in retinal degenerations. IUBMB Life 57 (2005) 381-388
18. Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., Hageman J.L., Stockman H.A., Borchardt J.D., Gehrs K.M., Smith R.J., Silvestri G., Russell S.R., Klaver C.C., Barbazetto I., Chang S., Yannuzzi L.A., Barile G.R., Merriam J.C., Smith R.T., Olsh A.K., Bergeron J., Zernant J., Merriam J.E., Gold B., Dean M., and Allikmets R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 7227-7232
19. Haider N.B., Demarco P., Nystuen A.M., Huang X., Smith R.S., McCall M.A., Naggert J.K., and Nishina P.M. The transcription factor Nr2e3 functions in retinal progenitors to suppress cone cell generation. Vis. Neurosci. 23 (2006) 917-929
20. Haider N.B., Jacobson S.G., Cideciyan A.V., Swiderski 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
21. 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
22. Haines J.L., Hauser M.A., Schmidt S., Scott W.K., Olson L.M., Gallins P., Spencer K.L., Kwan S.Y., Noureddine M., Gilbert J.R., Schnetz-Boutaud N., Agarwal A., Postel E.A., and Pericak-Vance M.A. Complement factor H variant increases the risk of age-related macular degeneration. Science 308 (2005) 419-421
23. Haston C.K., Cory S., Lafontaine L., Dorion G., and Hallett M.T. Strain-dependent pulmonary gene expression profiles of a cystic fibrosis mouse model. Physiol. Genom. 25 (2006) 336-345
24. 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
25. He Y.D., Dai H., Schadt E.E., Cavet G., Edwards S.W., Stepaniants S.B., Duenwald S., Kleinhanz R., Jones A.R., Shoemaker D.D., and Stoughton R.B. Microarray standard data set and figures of merit for comparing data processing methods and experiment designs. Bioinformatics 19 (2003) 956-965
26. Hughes T.R., Mao M., Jones A.R., Burchard J., Marton M.J., Shannon K.W., Lefkowitz S.M., Ziman M., Schelter J.M., Meyer M.R., Kobayashi S., Davis C., Dai H., He Y.D., Stepaniants S.B., Cavet G., Walker W.L., West A., Coffey E., Shoemaker D.D., Stoughton R.B., Blanchard A.P., Friend S.H., and Linsley P.S. Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat. Biotechnol. 19 (2001) 342-347
27. Iandiev I., Pannicke T., Reichel M.B., Wiedemann P., Reichenbach A., and Bringmann A. Expression of aquaporin-1 immunoreactivity by photoreceptor cells in the mouse retina. Neurosci. Lett. 388 (2005) 96-99
28. Jackson J.E. A User's Guide to Principal Components (2003), John Wiley & Sons, New York
29. Jamieson R.V., Perveen R., Kerr B., Carette M., Yardley J., Heon E., Wirth M.G., van Heyningen V., Donnai D., Munier F., and Black G.C. Domain disruption and mutation of the bZIP transcription factor, MAF, associated with cataract, ocular anterior segment dysgenesis and coloboma. Hum. Mol. Genet. 11 (2002) 33-42
30. Jones S.E., Jomary C., Grist J., Stewart H.J., and Neal M.J. Altered expression of secreted frizzled-related protein-2 in retinitis pigmentosa retinas. Invest. Ophthalmol. Vis. Sci. 41 (2000) 1297-1301
31. 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
32. Kedmi M., and Orr-Urtreger A. Differential brain transcriptome of beta4 nAChR subunit-deficient mice: is it the effect of the null mutation or the background strain?. Physiol. Genom. 28 (2007) 213-222
33. Klein R.J., Zeiss C., Chew E.Y., Tsai J.Y., Sackler R.S., Haynes C., Henning A.K., SanGiovanni J.P., Mane S.M., Mayne S.T., Bracken M.B., Ferris F.L., Ott J., Barnstable C., and Hoh J. Complement factor H polymorphism in age-related macular degeneration. Science 308 (2005) 385-389
34. Knupp C., Amin S.Z., Munro P.M., Luthert P.J., and Squire J.M. Collagen VI assemblies in age-related macular degeneration. J. Struct. Biol. 139 (2002) 181-189
35. Kobayashi M., Takezawa S.-I., 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
36. Livesey F.J., and Cepko C.L. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2 (2001) 109-118
37. Marquardt T. Transcriptional control of neuronal diversification in the retina. Prog. Retin. Eye Res. 22 (2003) 567-577
38. Marquardt T., and Gruss P. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci. 25 (2002) 32-38
39. Mears A.J., Kondo M., Swain P.K., Takada Y., Bush R.A., Saunders T.L., Sieving P.A., and Swaroop A. Nrl is required for rod photoreceptor development. Nat. Genet. 29 (2001) 447-452
40. 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
41. 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
42. 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
43. Reza H.M., and Yasuda K. Roles of Maf family proteins in lens development. Dev. Dyn. 229 (2004) 440-448
44. 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
45. Storm E.E., and Kingsley D.M. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122 (1996) 3969-3979
46. Vanita V., Singh D., Robinson P.N., Sperling K., and Singh J.R. A novel mutation in the DNA-binding domain of MAF at 16q23.1 associated with autosomal dominant "cerulean cataract" in an Indian family. Am. J. Med. Genet. A 140 (2006) 558-566
47. Vivat-Hannah V., Bourguet W., Gottardis M., and Gronemeyer H. Separation of retinoid X receptor homo- and heterodimerization functions. Mol. Cell. Biol. 23 (2003) 7678-7688
48. Wang Y., Barbacioru C., Hyland F., Xiao W., Hunkapiller K.L., Blake J., Chan F., Gonzalez C., Zhang L., and Samaha R.R. Large scale real-time PCR validation on gene expression measurements from two commercial long-oligonucleotide microarrays. BMC Genom 7 (2006) 59
49. Weng L., Dai H., Zhan Y., He Y., Stepaniants S.B., and Bassett D.E. Rosetta error model for gene expression analysis. Bioinformatics 22 (2006) 1111-1121
50. Wolkenberg 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
51. Yoshida S., Mears A.J., Friedman J.S., Carter T., He S., Oh E., Jing Y., Farjo R., Fleury G., Barlow C., Hero A.O., and 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. 13 (2004) 1487-1503
52. Yu J., He S., Friedman J.S., Akimoto M., Ghosh D., Mears A.J., Hicks D., and 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. 279 (2004) 42211-42220
53. Zareparsi S., Branham K.E., Li M., Shah S., Klein R.J., Ott J., Hoh J., Abecasis G.R., and Swaroop A. Strong association of the Y402H variant in complement factor H at 1q32 with susceptibility to age-related macular degeneration. Am. J. Hum. Genet. 77 (2005) 149-153