A global survey identifies novel upstream components of the Ath5 neurogenic network

Genome Biology

Volumn 10, Issue 9, 2009, Pages

  Souren, Marcel ^a   Martinez Morales, Juan R ^a,b   Makri, Panagiota ^a   Wittbrodt, Beate ^a   Wittbrodt, Joachim ^a  

^a Developmental Biology Unit   (Germany)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; LUCIFERASE; NEUROGENIN 3; TRANSCRIPTOME; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; EYE PROTEIN; FISH PROTEIN; HYBRID PROTEIN; NERVE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; IN VIVO STUDY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ORYZIAS; PROMOTER REGION; REGULATORY SEQUENCE; RETINA GANGLION CELL; ANIMAL; CELL LINE; CONFOCAL MICROSCOPY; CYTOLOGY; EYE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INNERVATION; METABOLISM; PRENATAL DEVELOPMENT; TIME;

VERTEBRATA;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; EYE; EYE PROTEINS; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; IN SITU HYBRIDIZATION, FLUORESCENCE; LUCIFERASES; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; ORYZIAS; RECOMBINANT FUSION PROTEINS; RETINAL GANGLION CELLS; TIME FACTORS; TRANSFECTION;

EID: 76249111774     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-9-r92     Document Type: Article

References (61)

1. Erwin D, Davidson E. The evolution of hierarchical gene regulatory networks. Nat Rev Genet 2009, 10:141-148. 10.1038/nrg2499, 19139764.
2. Mu X, Fu X, Sun H, Beremand PD, Thomas TL, Klein WH. A gene network downstream of transcription factor Math5 regulates retinal progenitor cell competence and ganglion cell fate. Dev Biol 2005, 280:467-481. 10.1016/j.ydbio.2005.01.028, 15882586.
3. Cremisi F, Philpott A, Ohnuma S. Cell cycle and cell fate interactions in neural development. Curr Opin Neurobiol 2003, 13:26-33. 10.1016/S0959-4388(03)00005-9, 12593979.
4. Livesey FJ, Cepko CL. Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2001, 2:109-118. 10.1038/35053522, 11252990.
5. Marquardt T, Gruss P. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 2002, 25:32-38. 10.1016/S0166-2236(00)02028-2, 11801336.
6. Ohnuma S, Harris WA. Neurogenesis and the cell cycle. Neuron 2003, 40:199-208. 10.1016/S0896-6273(03)00632-9, 14556704.
7. Del Bene F, Wehman AM, Link BA, Baier H. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 2008, 134:1055-1065. 10.1016/j.cell.2008.07.017, 2628487, 18805097.
8. Frade JM. Interkinetic nuclear movement in the vertebrate neuroepithelium: encounters with an old acquaintance. Prog Brain Res 2002, 136:67-71. full_text, 12143404.
9. Sauer FC. The interkinetic migration of embryonic epithelial nuclei. J Morphol 1936, 60:1-11.
10. Brown NL, Patel S, Brzezinski J, Glaser T. Math5 is required for retinal ganglion cell and optic nerve formation. Development 2001, 128:2497-2508. 1480839, 11493566.
11. Kay JN, Finger-Baier KC, Roeser T, Staub W, Baier H. Retinal ganglion cell genesis requires lakritz, a Zebrafish atonal homolog. Neuron 2001, 30:725-736. 10.1016/S0896-6273(01)00312-9, 11430806.
12. Wang SW, Kim BS, Ding K, Wang H, Sun D, Johnson RL, Klein WH, Gan L. Requirement for math5 in the development of retinal ganglion cells. Genes Dev 2001, 15:24-29. 10.1101/gad.855301, 312600, 11156601.
13. Kanekar S, Perron M, Dorsky R, Harris WA, Jan LY, Jan YN, Vetter ML. Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron 1997, 19:981-994. 10.1016/S0896-6273(00)80391-8, 9390513.
14. Liu W, Mo Z, Xiang M. The Ath5 proneural genes function upstream of Brn3 POU domain transcription factor genes to promote retinal ganglion cell development. Proc Natl Acad Sci USA 2001, 98:1649-1654. 10.1073/pnas.98.4.1649, 29311, 11172005.
15. Masai I, Yamaguchi M, Tonou-Fujimori N, Komori A, Okamoto H. The hedgehog-PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: the cell-cycle exit of retinoblasts and their neuronal maturation. Development 2005, 132:1539-1553. 10.1242/dev.01714, 15728672.
16. Poggi L, Vitorino M, Masai I, Harris WA. Influences on neural lineage and mode of division in the zebrafish retina in vivo . J Cell Biol 2005, 171:991-999. 10.1083/jcb.200509098, 2171316, 16365165.
17. Bonini NM, Choi KW. Early decisions in Drosophila eye morphogenesis. Curr Opin Genet Dev 1995, 5:507-515. 10.1016/0959-437X(95)90056-M, 7580144.
18. Hu M, Easter SS. Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev Biol 1999, 207:309-321. 10.1006/dbio.1998.9031, 10068465.
19. Masai I, Stemple DL, Okamoto H, Wilson SW. Midline signals regulate retinal neurogenesis in zebrafish. Neuron 2000, 27:251-263. 10.1016/S0896-6273(00)00034-9, 10985346.
20. Laessing U, Stuermer CA. Spatiotemporal pattern of retinal ganglion cell differentiation revealed by the expression of neurolin in embryonic zebrafish. J Neurobiol 1996, 29:65-74. 10.1002/(SICI)1097-4695(199601)29:1<65::AID-NEU5>3.0.CO;2-5, 8748372.
21. Prada C, Puga J, Perez-Mendez L, Lopez R, Ramirez G. Spatial and temporal patterns of neurogenesis in the chick retina. Eur J Neurosci 1991, 3:559-569. 10.1111/j.1460-9568.1991.tb00843.x, 12106488.
22. Young RW. Cell differentiation in the retina of the mouse. Anat Rec 1985, 212:199-205. 10.1002/ar.1092120215, 3842042.
23. Esteve P, Trousse F, Rodriguez J, Bovolenta P. SFRP1 modulates retina cell differentiation through a beta-catenin-independent mechanism. J Cell Sci 2003, 116:2471-2481. 10.1242/jcs.00452, 12724355.
24. Martinez-Morales JR, Del Bene F, Nica G, Hammerschmidt M, Bovolenta P, Wittbrodt J. Differentiation of the vertebrate retina is coordinated by an FGF signaling center. Dev Cell 2005, 8:565-574. 10.1016/j.devcel.2005.01.022, 15809038.
25. Shkumatava A, Fischer S, Muller F, Strahle U, Neumann CJ. Sonic hedgehog, secreted by amacrine cells, acts as a short-range signal to direct differentiation and lamination in the zebrafish retina. Development 2004, 131:3849-3858. 10.1242/dev.01247, 15253932.
26. Vinothkumar S, Rastegar S, Takamiya M, Ertzer R, Strahle U. Sequential and cooperative action of Fgfs and Shh in the zebrafish retina. Dev Biol 2008, 314:200-214. 10.1016/j.ydbio.2007.11.034, 18177854.
27. Kay JN, Link BA, Baier H. Staggered cell-intrinsic timing of ath5 expression underlies the wave of ganglion cell neurogenesis in the zebrafish retina. Development 2005, 132:2573-2585. 10.1242/dev.01831, 15857917.
28. Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, Kageyama R. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 2004, 131:5539-5550. 10.1242/dev.01436, 15496443.
29. Tomita K, Ishibashi M, Nakahara K, Ang SL, Nakanishi S, Guillemot F, Kageyama R. Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 1996, 16:723-734. 10.1016/S0896-6273(00)80093-8, 8607991.
30. Matter-Sadzinski L, Puzianowska-Kuznicka M, Hernandez J, Ballivet M, Matter JM. A bHLH transcriptional network regulating the specification of retinal ganglion cells. Development 2005, 132:3907-3921. 10.1242/dev.01960, 16079155.
31. Del Bene F, Ettwiller L, Skowronska-Krawczyk D, Baier H, Matter JM, Birney E, Wittbrodt J. In vivo validation of a computationally predicted conserved Ath5 target gene set. PLoS Genet 2007, 3:1661-1671. 10.1371/journal.pgen.0030159, 1988851,1988851, 17892326.
32. Skowronska-Krawczyk D, Ballivet M, Dynlacht BD, Matter JM. Highly specific interactions between bHLH transcription factors and chromatin during retina development. Development 2004, 131:4447-4454. 10.1242/dev.01302, 15342472.
33. Hernandez J, Matter-Sadzinski L, Skowronska-Krawczyk D, Chiodini F, Alliod C, Ballivet M, Matter JM. Highly conserved sequences mediate the dynamic interplay of basic helix-loop-helix proteins regulating retinogenesis. J Biol Chem 2007, 282:37894-37905. 10.1074/jbc.M703616200, 17971452.
34. Hufnagel RB, Riesenberg AN, Saul SM, Brown NL. Conserved regulation of Math5 and Math1 revealed by Math5-GFP transgenes. Mol Cell Neurosci 2007, 36:435-448. 10.1016/j.mcn.2007.08.006, 2095782, 17900924.
35. Riesenberg AN, Le TT, Willardsen MI, Blackburn DC, Vetter ML, Brown NL. Pax6 regulation of Math5 during mouse retinal neurogenesis. Genesis 2009, 47:175-187. 10.1002/dvg.20479, 19208436.
36. Willardsen MI, Suli A, Pan Y, Marsh-Armstrong N, Chien CB, El-Hodiri H, Brown NL, Moore KB, Vetter ML. Temporal regulation of Ath5 gene expression during eye development. Dev Biol 2009, 326:471-481. 10.1016/j.ydbio.2008.10.046, 19059393.
37. Deplancke B, Dupuy D, Vidal M, Walhout AJ. A gateway-compatible yeast one-hybrid system. Genome Res 2004, 14:2093-2101. 10.1101/gr.2445504, 528925, 15489331.
38. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Pena-Castillo L, Alleyne TM, Mnaimneh S, Botvinnik OB, Chan ET, Khalid F, Zhang W, Newburger D, Jaeger SA, Morris QD, Bulyk ML, Hughes TR. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008, 133:1266-1276. 10.1016/j.cell.2008.05.024, 2531161, 18585359.
39. Noyes MB, Christensen RG, Wakabayashi A, Stormo GD, Brodsky MH, Wolfe SA. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 2008, 133:1277-1289. 10.1016/j.cell.2008.05.023, 2478728, 18585360.
40. Liu Y, Kern JT, Walker JR, Johnson JA, Schultz PG, Luesch H. A genomic screen for activators of the antioxidant response element. Proc Natl Acad Sci USA 2007, 104:5205-5210. 10.1073/pnas.0700898104, 1829287, 17360324.
41. Fan F, Wood KV. Bioluminescent assays for high-throughput screening. Assay Drug Dev Technol 2007, 5:127-136. 10.1089/adt.2006.053, 17355205.
42. Boutros M, Brás LP, Huber W. Analysis of cell-based RNAi screens. Genome Biol 2006, 7:R66. 10.1186/gb-2006-7-7-r66, 1779553, 16869968.
43. Medaka Expression Pattern Database. , http://ani.embl.de:8080/mepd/
44. Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Münch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E. TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 2003, 31:374-378. 10.1093/nar/gkg108, 165555, 12520026.
45. Okuda T, Kokame K, Miyata T. Differential expression patterns of NDRG family proteins in the central nervous system. J Histochem Cytochem 2008, 56:175-182. 10.1369/jhc.7A7323.2007, 2324175, 17998568.
46. Rembold M, Lahiri K, Foulkes NS, Wittbrodt J. Transgenesis in fish: efficient selection of transgenic fish by co-injection with a fluorescent reporter construct. Nat Protoc 2006, 1:1133-1139. 10.1038/nprot.2006.165, 17406394.
47. Stathopoulos A, Levine M. Genomic regulatory networks and animal development. Dev Cell 2005, 9:449-462. 10.1016/j.devcel.2005.09.005, 16198288.
48. Levine M, Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151. 10.1038/nature01763, 12853946.
49. Noseda M, Niessen K, McLean G, Chang L, Karsan A. Notch-dependent cell cycle arrest is associated with downregulation of minichromosome maintenance proteins. Circ Res 2005, 97:102-104. 10.1161/01.RES.0000174380.06673.81, 15976316.
50. Chen D, Opavsky R, Pacal M, Tanimoto N, Wenzel P, Seeliger MW, Leone G, Bremner R. Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biol 2007, 5:e179. 10.1371/journal.pbio.0050179, 1914394, 17608565.
51. Keller SA, Ullah Z, Buckley MS, Henry RW, Arnosti DN. Distinct developmental expression of Drosophila retinoblastoma factors. Gene Expr Patterns 2005, 5:411-421. 10.1016/j.modgep.2004.09.005, 15661648.
52. Yang Z, Ding K, Pan L, Deng M, Gan L. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol 2003, 264:240-254. 10.1016/j.ydbio.2003.08.005, 14623245.
53. Merz C, Urlaub H, Will CL, Luhrmann R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 2007, 13:116-128. 10.1261/rna.336807, 1705747, 17095540.
54. Yamaguchi M, Tonou-Fujimori N, Komori A, Maeda R, Nojima Y, Li H, Okamoto H, Masai I. Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 2005, 132:3027-3043. 10.1242/dev.01881, 15944187.
55. Koster R, Stick R, Loosli F, Wittbrodt J. Medaka spalt acts as a target gene of hedgehog signaling. Development 1997, 124:3147-3156.
56. Iwamatsu T. Stages of normal development in the medaka Oryzias latipes . Mech Dev 2004, 121:605-618. 10.1016/j.mod.2004.03.012, 15210170.
57. Loosli F, Koster RW, Carl M, Kuhnlein R, Henrich T, Mucke M, Krone A, Wittbrodt J. A genetic screen for mutations affecting embryonic development in medaka fish (Oryzias latipes). Mech Dev 2000, 97:133-139. 10.1016/S0925-4773(00)00406-8, 11025214.
58. Loosli F, Winkler S, Burgtorf C, Wurmbach E, Ansorge W, Henrich T, Grabher C, Arendt D, Carl M, Krone A, Grzebisz E, Wittbrodt J. Medaka eyeless is the key factor linking retinal determination and eye growth. Development 2001, 128:4035-4044.
59. Loosli F, Koster RW, Carl M, Krone A, Wittbrodt J. Six3, a medaka homologue of the Drosophila homeobox gene sine oculis is expressed in the anterior embryonic shield and the developing eye. Mech Dev 1998, 74:159-164. 10.1016/S0925-4773(98)00055-0, 9651515.
60. Possum web page. , http://zlab.bu.edu/~mfrith/possum/
61. Martinez-Morales JR, Rembold M, Greger K, Simpson JC, Brown KE, Quiring R, Pepperkok R, Martin-Bermudo MD, Himmelbauer H, Wittbrodt J. ojoplano-mediated basal constriction is essential for optic cup morphogenesis. Development 2009, 136:2165-2175. 10.1242/dev.033563, 19502481.