An essential role for RAX homeoprotein and NOTCH-HES signaling in Otx2 expression in embryonic retinal photoreceptor cell fate determination

Journal of Neuroscience

Volumn 31, Issue 46, 2011, Pages 16792-16807

  Muranishi, Yuki ^a   Terada, Koji ^a,e   Inoue, Tatsuya ^a,c   Katoh, Kimiko ^a,b   Tsujii, Toshinori ^a   Sanuki, Rikako ^a,b   Kurokawa, Daisuke ^d   Aizawa, Shinichi ^d   Tamaki, Yasuhiro ^c   Furukawa, Takahisa ^a,b  

^a OSAKA BIOSCIENCE INSTITUTE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d RIKEN   (Japan)

^e HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; NOTCH RECEPTOR; RAX PROTEIN; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL FATE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC ENHANCER LOCUS OF PHOTORECEPTOR OTX2 TRANSCRIPTION; ENHANCER REGION; FEMALE; GENE INACTIVATION; IN VIVO STUDY; MOUSE EMBRYO; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BROMODEOXYURIDINE; CELL CYCLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; EMBRYO, MAMMALIAN; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGENESIS; ORGAN CULTURE TECHNIQUES; OTX TRANSCRIPTION FACTORS; PHOTORECEPTOR CELLS, VERTEBRATE; PREGNANCY; RECEPTORS, NOTCH; RETINA; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 81255142987     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3109-11.2011     Document Type: Article

References (52)

1. Akagi T, Inoue T, Miyoshi G, Bessho Y, Takahashi M, Lee JE, Guillemot F, Kageyama R (2004) Requirement of multiple basic helix-loop-helix genes for retinal neuronal subtype specification. J Biol Chem 279:28492-28498.
2. Alexiades MR, Cepko C (1996) Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 205:293-307.
3. Baye LM, Link BA (2007) Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27:10143-10152.
4. Cayouette M, Raff M (2003) The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development 130:2329-2339.
5. Chen CM, Cepko CL (2002) The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development 129:5363-5375.
6. Chuang JC, Mathers PH, Raymond PA (1999) Expression of three Rx homeobox genes in embryonic and adult zebrafish. Mech Dev 84:195-198.
7. Del Bene F, Wehman AM, Link BA, Baier H (2008) Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134:1055-1065.
8. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84:911-921.
9. Dyer MA, Livesey FJ, Cepko CL, Oliver G (2003) Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet 34:53-58.
10. Feil R, Wagner J, Metzger D, Chambon P (1997) Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237:752-757.
11. Fischer A, Gessler M (2007) Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res 35:4583-4596.
12. Furukawa A, Koike C, Lippincott P, Cepko CL, Furukawa T (2002) The mouse Crx 5'-upstream transgene sequence directs cell-specific and developmentally regulated expression in retinal photoreceptor cells. J Neurosci 22:1640-1647.
13. Furukawa T, Kozak CA, Cepko CL (1997) Rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc Natl Acad Sci U S A 94:3088-3093.
14. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL (2000) Rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394.
15. Gong S, Yang XW, Li C, Heintz N (2002) Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6Kgamma origin of replication. Genome Res 12:1992-1998.
16. Hojo M, Ohtsuka T, Hashimoto N, Gradwohl G, Guillemot F, Kageyama R (2000) Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127:2515-2522.
17. Holt CE, Bertsch TW, Ellis HM, Harris WA (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15-26.
18. Hufnagel RB, Le TT, Riesenberg AL, Brown NL (2010) Neurog2 controls the leading edge of neurogenesis in the mammalian retina. Dev Biol 340:490-503.
19. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194:237-255.
20. Jadhav AP, Mason HA, Cepko CL (2006) Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133:913-923.
21. Katoh K, Omori Y, Onishi A, Sato S, Kondo M, Furukawa T (2010) Blimp1 suppresses Chx10 expression in differentiating retinal photoreceptor precursors to ensure proper photoreceptor development. J Neurosci 30:6515-6526.
22. Koike C, Nishida A, Ueno S, Saito H, Sanuki R, Sato S, Furukawa A, Aizawa S, Matsuo I, Suzuki N, Kondo M, Furukawa T (2007) Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol Cell Biol 27:8318-8329.
23. Kothary R, Clapoff S, Darling S, Perry MD, Moran LA, Rossant J (1989) Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105:707-714.
24. Kurokawa D, Takasaki N, Kiyonari H, Nakayama R, Kimura-Yoshida C, Matsuo I, Aizawa S (2004a) Regulation of Otx2 expression and its functions in mouse epiblast and anterior neuroectoderm. Development 131:3307-3317.
25. Kurokawa D, Kiyonari H, Nakayama R, Kimura-Yoshida C, Matsuo I, Aizawa S (2004b) Regulation of Otx2 expression and its functions in mouse forebrain and midbrain. Development 131:3319-3331.
26. Levine EM, Green ES (2004) Cell-intrinsic regulators of proliferation in vertebrate retinal progenitors. Semin Cell Dev Biol 15:63-74.
27. Livesey FJ, Cepko CL (2001) Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2:109-118.
28. Mathers PH, Grinberg A, Mahon KA, Jamrich M (1997) The Rx homeobox gene is essential for vertebrate eye development. Nature 387:603-607.
29. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
30. Muranishi Y, Sato S, Inoue T, Ueno S, Koyasu T, Kondo M, Furukawa T (2010) Gene expression analysis of embryonic photoreceptor precursor cells using BAC-Crx-EGFP transgenic mouse. Biochem Biophys Res Commun 392:317-322.
31. Nelson SM, Park L, Stenkamp DL (2009) Retinal homeobox 1 is required for retinal neurogenesis and photoreceptor differentiation in embryonic zebrafish. Dev Biol 328:24-39.
32. Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, Matsuo I, Furukawa T (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 6:1255-1263.
33. Ohsawa R, KageyamaR (2008) Regulation of retinal cell fate specification by multiple transcription factors. Brain Res 1192:90-98.
34. Pan Y, Martinez-De Luna RI, Lou CH, Nekkalapudi S, Kelly LE, Sater AK, El-Hodiri HM (2010) Regulation of photoreceptor gene expression by the retinal homeobox (Rx) gene product. Dev Biol 339:494-506.
35. Riesenberg AN, Liu Z, Kopan R, Brown NL (2009) Rbpj cell autonomous regulation of retinal ganglion cell and cone photoreceptor fates in the mouse retina. J Neurosci 29:12865-12877.
36. Sakai K, Miyazaki J (1997) A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the cre transgene transmission. Biochem Biophys Res Commun 237:318-324.
37. Sanuki R, Omori Y, Koike C, Sato S, (2010) Panky, a novel photoreceptor-specific ankyrin repeat protein, is a transcriptional cofactor that suppresses CRX-regulated photoreceptor genes. FEBS Lett 584:753-758.
38. Sato S, Inoue T, Terada K, Matsuo I, Aizawa S, Tano Y, Fujikado T, Furukawa T (2007) Dkk3-Cre BAC transgenic mouse line: a tool for highly efficient gene deletion in retinal progenitor cells. Genesis 45:502-507.
39. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923-931.
40. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852.
41. Takatsuka K, Hatakeyama J, Bessho Y, Kageyama R (2004) Roles of the bHLH gene Hes1 in retinal morphogenesis. Brain Res 1004:148-155.
42. Tian E, Kimura C, Takeda N, Aizawa S, Matsuo I (2002) Otx2 is required to respond to signals from anterior neural ridge for forebrain specification. Dev Biol 242:204-223.
43. Trimarchi JM, Stadler MB, Cepko CL (2008) Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS One 3:e1588
44. Turner DL, Cepko CL (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131-136.
45. Turner DL, Snyder EY, Cepko CL (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4:833-845.
46. Walsh C, Cepko CL (1988) Clonally related cortical cells show several migration patterns. Science 241:1342-1345.
47. Walsh C, Cepko CL (1993) Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362:632-635.
48. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142-1145.
49. Wilson D, Sheng G, Lecuit T, Dostatni N, Desplan C (1993) Cooperative dimerization of paired class homeo domains on DNA. Genes Dev 7:2120-2134.
50. Yang XW, Model P, Heintz N (1997) Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865.
51. Yaron O, Farhy C, Marquardt T, Applebury M, Ashery-Padan R (2006) Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133:1367-1378.
52. Zheng MH, Shi M, Pei Z, Gao F, Han H, Ding YQ (2009) The transcription factor RBP-J is essential for retinal cell differentiation and lamination. Mol Brain 2:38