A gene regulatory network controls the binary fate decision of rod and bipolar cells in the vertebrate retina

Developmental Cell

Volumn 30, Issue 5, 2014, Pages 513-527

  Wang, Sui ^a,b   Sengel, Cem ^a   Emerson, Mark M ^c   Cepko, Constance L ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; RETINOID RELATED ORPHAN RECEPTOR BETA; TRANSCRIPTION FACTOR OTX2; HOMEODOMAIN PROTEIN; NOTCH1 PROTEIN, MOUSE; NOTCH1 RECEPTOR; OTX2 PROTEIN, MOUSE; PRDM1 PROTEIN, MOUSE; RORB PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OTX; VSX2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL FATE; CONTROLLED STUDY; ELECTROPORATION; GENE REGULATORY NETWORK; IN VIVO STUDY; MOUSE; NEGATIVE FEEDBACK; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA BIPOLAR GANGLION CELL; RETINA ROD; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; ENHANCER REGION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION REGULATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA;

MAMMALIA; MURINAE; VERTEBRATA;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 2; OTX TRANSCRIPTION FACTORS; RECEPTOR, NOTCH1; RETINA; RETINAL BIPOLAR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; TRANSCRIPTION FACTORS;

EID: 84908612662     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.07.018     Document Type: Article

References (65)

1. Afelik S., Jensen J. Notch signaling in the pancreas: patterning and cell fate specification. Wiley interdisciplinary reviews. Dev. Biol. 2013, 2:531-544.
2. Arnone M.I., Davidson E.H. The hardwiring of development: organization and function of genomic regulatory systems. Development 1997, 124:1851-1864.
3. Berman B.P., Nibu Y., Pfeiffer B.D., Tomancak P., Celniker S.E., Levine M., Rubin G.M., Eisen M.B. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 2002, 99:757-762.
4. Billings N.A., Emerson M.M., Cepko C.L. Analysis of thyroid response element activity during retinal development. PLoS ONE 2010, 5:e13739.
5. Boucherie C., Sowden J.C., Ali R.R. Induced pluripotent stem cell technology for generating photoreceptors. Regen. Med. 2011, 6:469-479.
6. Bramblett D.E., Pennesi M.E., Wu S.M., Tsai M.-J. The transcription factor Bhlhb4 is required for rod bipolar cell maturation. Neuron 2004, 43:779-793.
7. Brzezinski J.A., Lamba D.A., Reh T.A. Blimp1 controls photoreceptor versus bipolar cell fate choice during retinal development. Development 2010, 137:619-629.
8. Brzezinski J.A., Uoon Park K., Reh T.A. Blimp1 (Prdm1) prevents re-specification of photoreceptors into retinal bipolar cells by restricting competence. Dev. Biol. 2013, 384:194-204.
9. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 2012, 28:276-284.
10. Burmeister M., Novak J., Liang M.Y., Basu S., Ploder L., Hawes N.L., Vidgen D., Hoover F., Goldman D., Kalnins V.I., et al. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 1996, 12:376-384.
11. Cherry T., Wang S., Bormuth I., Schwab M., Olson J., Cepko C. NeuroD factors regulate cell fate and neurite stratification in the developing retina. J.Neurosci. 2011, 31:7365-7379.
12. Chow L., Levine E., Reh T. The nuclear receptor transcription factor, retinoid-related orphan receptor beta, regulates retinal progenitor proliferation. Mech. Dev 1998, 77:149-164.
13. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
14. DeKoter R.P., Singh H. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 2000, 288:1439-1441.
15. Emerson M.M., Cepko C.L. Identification of a retina-specific Otx2 enhancer element active in immature developing photoreceptors. Dev. Biol. 2011, 360:241-255.
16. Fossat N., Le Greneur C., Béby F., Vincent S., Godement P., Chatelain G., Lamonerie T. A new GFP-tagged line reveals unexpected Otx2 protein localization in retinal photoreceptors. BMC Dev. Biol. 2007, 7:122.
17. Graf T., Enver T. Forcing cells to change lineages. Nature 2009, 462:587-594.
18. Hafler B.P., Surzenko N., Beier K.T., Punzo C., Trimarchi J.M., Kong J.H., Cepko C.L. Transcription factor Olig2 defines subpopulations ofretinal progenitor cells biased toward specific cell fates. Proc. Natl. Acad. Sci. USA 2012, 109:7882-7887.
19. Jadhav A.P., Mason H.A., Cepko C.L. Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 2006, 133:913-923.
20. Jia L., Oh E.C., Ng L., Srinivas M., Brooks M., Swaroop A., Forrest D. Retinoid-related orphan nuclear receptor RORbeta is an early-acting factor in rod photoreceptor development. Proc. Natl. Acad. Sci. USA 2009, 106:17534-17539.
21. John S.A., Garrett-Sinha L.A. Blimp1: a conserved transcriptional repressor critical for differentiation of many tissues. Exp. Cell Res. 2009, 315:1077-1084.
22. Jukam D., Desplan C. Binary fate decisions in differentiating neurons. Curr. Opin. Neurobiol. 2010, 20:6-13.
23. Kamachi Y., Kondoh H. Sox proteins: regulators of cell fate specification and differentiation. Development 2013, 140:4129-4144.
24. Katoh K., Omori Y., Onishi A., Sato S., Kondo M., Furukawa T. Blimp1 suppresses Chx10 expression in differentiating retinal photoreceptor precursors to ensure proper photoreceptor development. J.Neurosci. 2010, 30:6515-6526.
25. Kim D., Matsuda T., Cepko C. A core paired-type and POU homeodomain-containing transcription factor program drives retinal bipolar cell gene expression. J.Neurosci. 2008, 28:7748-7764.
26. Kim D.S., Ross S.E., Trimarchi J.M., Aach J., Greenberg M.E., Cepko C.L. Identification of molecular markers of bipolar cells in the murine retina. J.Comp. Neurol. 2008, 507:1795-1810.
27. Koike C., Nishida A., Ueno S., Saito H., Sanuki R., Sato S., Furukawa A., Aizawa S., Matsuo I., Suzuki N., et al. Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol. Cell. Biol. 2007, 27:8318-8329.
28. La Torre A., Georgi S., Reh T.A. Conserved microRNA pathway regulates developmental timing of retinal neurogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:E2362-E2370.
29. Lee S.K., Pfaff S.L. Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 2001, 4(Suppl):1183-1191.
30. Livesey F.J., Cepko C.L. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2001, 2:109-118.
31. Livne-Bar I., Pacal M., Cheung M.C., Hankin M., Trogadis J., Chen D., Dorval K.M., Bremner R. Chx10 is required to block photoreceptor differentiation but is dispensable for progenitor proliferation in the postnatal retina. Proc. Natl. Acad. Sci. USA 2006, 103:4988-4993.
32. Loots G.G., Ovcharenko I. rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucleic Acids Res. 2004, 32:W217-W221.
33. Magnúsdóttir E., Kalachikov S., Mizukoshi K., Savitsky D., Ishida-Yamamoto A., Panteleyev A.A., Calame K. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. USA 2007, 104:14988-14993.
34. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
35. Masland R.H., Raviola E. Confronting complexity: strategies forunderstanding the microcircuitry of the retina. Annu. Rev. Neurosci. 2000, 23:249-284.
36. Matsuda T., Cepko C.L. Electroporation and RNA interference in the rodent retina invivo and invitro. Proc. Natl. Acad. Sci. USA 2004, 101:16-22.
37. Matsuda T., Cepko C.L. Controlled expression of transgenes introduced by invivo electroporation. Proc. Natl. Acad. Sci. USA 2007, 104:1027-1032.
38. Matys V., Kel-Margoulis O.V., Fricke E., Liebich I., Land S., Barre-Dirrie A., Reuter I., Chekmenev D., Krull M., Hornischer K., et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 2006, 34:D108-D110.
39. Meister M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 1996, 93:609-614.
40. Mizeracka K., DeMaso C.R., Cepko C.L. Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate. Development 2013, 140:3188-3197.
41. Mizeracka K., Trimarchi J., Stadler M., Cepko C. Analysis ofgene expression in wild-type and Notch1 mutant retinal cells by single cell profiling. Dev. Dyn. 2013, 242:1147-1159.
42. Morrow E.M., Furukawa T., Lee J.E., Cepko C.L. NeuroD regulates multiple functions in the developing neural retina in rodent. Development 1999, 126:23-36.
43. Muzumdar M., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
44. Nakajima H. Role of transcription factors in differentiation and reprogramming of hematopoietic cells. Keio J. Med. 2011, 60:47-55.
45. Nie K., Gomez M., Landgraf P., Garcia J.-F.F., Liu Y., Tan L.H., Chadburn A., Tuschl T., Knowles D.M., Tam W. MicroRNA-mediated down-regulation of PRDM1/Blimp-1 in Hodgkin/Reed-Sternberg cells: a potential pathogenetic lesion in Hodgkin lymphomas. Am. J. Pathol. 2008, 173:242-252.
46. 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.
47. Ohsawa R., Kageyama R. Regulation of retinal cell fate specification by multiple transcription factors. Brain Res. 2008, 1192:90-98.
48. Ong J.M., da Cruz L. A review and update on the current status ofstem cell therapy and the retina. Br. Med. Bull. 2012, 102:133-146.
49. Qiu L., Wang H., Xia X., Zhou H., Xu Z. A construct with fluorescent indicators for conditional expression of miRNA. BMC Biotechnol. 2008, 8:77.
50. Raj A., van Oudenaarden A. Single-molecule approaches to stochastic gene expression. Annu. Rev. Biophys. 2009, 38:255-270.
51. Sato S., Inoue T., Terada K., Matsuo I., Aizawa S., Tano Y., Fujikado T., Furukawa T. Dkk3-Cre BAC transgenic mouse line: a tool for highly efficient gene deletion in retinal progenitor cells. Genesis 2007, 45:502-507.
52. Sigvardsson M. Transcription factor dose links development to disease. Blood 2012, 120:3630-3631.
53. Smith J., Theodoris C., Davidson E.H. A gene regulatory network subcircuit drives a dynamic pattern of gene expression. Science 2007, 318:794-797.
54. Sternberg S.H., Redding S., Jinek M., Greene E.C., Doudna J.A. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 2014, 507:62-67.
55. Struhl G., Johnston P., Lawrence P.A. Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 1992, 69:237-249.
56. Taranova O.V., Magness S.T., Fagan B.M., Wu Y., Surzenko N., Hutton S.R., Pevny L.H. SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 2006, 20:1187-1202.
57. Trimarchi J.M., Stadler M.B., Cepko C.L. Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS ONE 2008, 3:e1588.
58. Turner D.L., Cepko C.L. A common progenitor for neurons and glia persists in rat retina late in development. Nature 1987, 328:131-136.
59. Wang S., Yan J., Anderson D.A., Xu Y., Kanal M.C., Cao Z., Wright C.V., Gu G. Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev. Biol. 2010, 339:26-37.
60. Wasserman W.W., Fickett J.W. Identification of regulatory regions which confer muscle-specific gene expression. J.Mol. Biol. 1998, 278:167-181.
61. West J.A., Viswanathan S.R., Yabuuchi A., Cunniff K., Takeuchi A., Park I.-H.H., Sero J.E., Zhu H., Perez-Atayde A., Frazier A.L., et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 2009, 460:909-913.
62. Yaron O., Farhy C., Marquardt T., Applebury M., Ashery-Padan R. Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 2006, 133:1367-1378.
63. Young R.W. Cell differentiation in the retina of the mouse. Anat. Rec. 1985, 212:199-205.
64. Young R.W. Cell proliferation during postnatal development of the retina in the mouse. Brain Res. 1985, 353:229-239.
65. Zhang L., Stokes N., Polak L., Fuchs E. Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment. Cell Stem Cell 2011, 8:294-308.