Notch-Delta signaling is required for spatial patterning and Müller glia differentiation in the zebrafish retina

Developmental Biology

Volumn 278, Issue 2, 2005, Pages 381-395

  Bernardos, R L ^a   Lentz, S I ^b   Wolfe, M S ^c   Raymond, P A ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Delta; Hes; mind bomb; M ller glia; Notch; Photoreceptors; Retinal development; secretase inhibitors her

Indexed keywords

GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; UBIQUITIN PROTEIN LIGASE;

ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; ENZYME INACTIVATION; MUELLER CELL; NONHUMAN; PHOTORECEPTOR CELL; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; RETINA CONE; RETINA DEVELOPMENT;

DANIO RERIO; VERTEBRATA;

EID: 12944299273     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.11.018     Document Type: Article

References (82)

1. I. Ahmad, A.V. Das, J. James, S. Bhattacharya, and X. Zhao Neural stem cells in the mammalian eye: types and regulation Semin. Cell Dev. Biol. 15 2004 53 62
2. C. Andressen, I. Blumcke, and M.R. Celio Calcium-binding proteins: selective markers of nerve cells Cell Tissue Res. 271 1993 181 208
3. C.P. Austin, D.E. Feldman, J.A. Ida Jr., and C.L. Cepko Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch Development 121 1995 3637 3650
4. N.E. Baker, and A.E. Zitron Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous Mech. Dev. 49 1995 173 189
5. Z.Z. Bao, and C.L. Cepko The expression and function of Notch pathway genes in the developing rat eye J. Neurosci. 17 1997 1425 1434
6. M. Baron An overview of the Notch signalling pathway Semin. Cell Dev. Biol. 14 2003 113 119
7. L.K. Barthel, and P.A. Raymond Improved method for obtaining 3-microns cryosections for immunocytochemistry J. Histochem. Cytochem. 38 1990 1383 1388
8. L.K. Barthel, and P.A. Raymond Subcellular localization of alpha-tubulin and opsin mRNA in the goldfish retina using digoxigenin-labeled cRNA probes detected by alkaline phosphatase and HRP histochemistry J. Neurosci. Methods 50 1993 145 152
9. L.K. Barthel, and P.A. Raymond In situ hybridization studies of retinal neurons Methods Enzymol. 316 2000 579 590
10. K. Basler, and E. Hafen Specification of cell fate in the developing eye of Drosophila BioEssays 13 1991 621 631
11. C.E. Bland, P. Kimberly, and M.D. Rand Notch-induced proteolysis and nuclear localization of the Delta ligand J. Biol. Chem. 278 2003 13607 13610
12. T. Branchek, and R. Bremiller The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure J. Comp. Neurol. 224 1984 107 115
13. C.A. Brennan, and K. Moses Determination of Drosophila photoreceptors: timing is everything Cell. Mol. Life Sci. 57 2000 195 214
14. J.D. Burrill, and S.S. Easter Jr. Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio) J. Comp. Neurol. 346 1994 583 600
15. B. De Strooper, and W. Annaert Proteolytic processing and cell biological functions of the amyloid precursor protein J. Cell Sci. 113 Pt. 11 2000 1857 1870
16. B. De Strooper, W. Annaert, P. Cupers, P. Saftig, K. Craessaerts, J.S. Mumm, E.H. Schroeter, V. Schrijvers, M.S. Wolfe, W.J. Ray, A. Goate, and R. Kopan A presenilin-1-dependent gamma-secretes-like protease mediates release of Notch intracellular domain Nature 398 1999 518 522
17. R.I. Dorsky, W.S. Chang, D.H. Rapaport, and W.A. Harris Regulation of neuronal diversity in the Xenopus retina by Delta signalling Nature 385 1997 67 70
18. J.O. Ebinu, and B.A. Yankner A RIP tide in neuronal signal transduction Neuron 34 2002 499 502
19. B. Erdmann, F.P. Kirsch, F.G. Rathjen, and M.I. More N-cadherin is essential for retinal lamination in the zebrafish Dev. Dyn. 226 2003 570 577
20. J.M. Fadool Development of a rod photoreceptor mosaic revealed in transgenic zebrafish Dev. Biol. 258 2003 277 290
21. D. Fashena, and M. Westerfield Secondary motoneuron axons localize DM-GRASP on their fasciculated segments J. Comp. Neurol. 406 1999 415 424
22. M.E. Fortini Gamma-secretase-mediated proteolysis in cell-surface- receptor signalling Nat. Rev., Mol. Cell Biol. 3 2002 673 684
23. T. Furukawa, S. Mukherjee, Z.Z. Bao, E.M. Morrow, and C.L. Cepko rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells Neuron 26 2000 383 394
24. N. Gaiano, and G. Fishell The role of notch in promoting glial and neural stem cell fates Annu. Rev. Neurosci. 25 2002 471 490
25. N. Gaiano, J.S. Nye, and G. Fishell Radial glial identity is promoted by Notch1 signaling in the murine forebrain Neuron 26 2000 395 404
26. A. Geling, H. Steiner, M. Willem, L. Bally-Cuif, and C. Haass A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish EMBO Rep. 3 2002 688 694
27. C. Haddon, Y.J. Jiang, L. Smithers, and J. Lewis Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant Development 125 1998 4637 4644
28. J. Hatakeyama, and R. Kageyama Retinal cell fate determination and bHLH factors Semin. Cell Dev. Biol. 15 2004 83 89
29. M. Hojo, T. Ohtsuka, N. Hashimoto, G. Gradwohl, F. Guillemot, and R. Kageyama Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina Development 127 2000 2515 2522
30. M. Hu, and S.S. Easter Retinal neurogenesis: the formation of the initial central patch of postmitotic cells Dev. Biol. 207 1999 309 321
31. T. Ikeuchi, and S.S. Sisodia The Notch ligands, Delta1 and Jagged2, are substrates for presenilin-dependent "gamma-secretase" cleavage J. Biol. Chem. 278 2003 7751 7754
32. T. Iso, L. Kedes, and Y. Hamamori HES and HERP families: multiple effectors of the Notch signaling pathway J. Cell. Physiol. 194 2003 237 255
33. M. Itoh, C.H. Kim, G. Palardy, T. Oda, Y.J. Jiang, D. Maust, S.Y. Yeo, K. Lorick, G.J. Wright, L. Ariza-McNaughton, A.M. Weissman, J. Lewis, S.C. Chandrasekharappa, and A.B. Chitnis Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta Dev. Cell 4 2003 67 82
34. Y.J. Jiang, M. Brand, C.P. Heisenberg, D. Beuchle, M. Furutani-Seiki, R.N. Kelsh, R.M. Warga, M. Granato, P. Haffter, M. Hammerschmidt, D.A. Kane, M.C. Mullins, J. Odenthal, F.J. van Eeden, and C. Nusslein-Volhard Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio Development 123 1996 205 216
35. N.J. Justice, and Y.N. Jan Variations on the Notch pathway in neural development Curr. Opin. Neurobiol. 12 2002 64 70
36. R. Kageyama, and T. Ohtsuka The Notch-Hes pathway in mammalian neural development Cell Res. 9 1999 179 188
37. R. Kageyama, M. Ishibashi, K. Takebayashi, and K. Tomita bHLH transcription factors and mammalian neuronal differentiation Int. J. Biochem. Cell Biol. 29 1997 1389 1399
38. W.T. Kimberly, and M.S. Wolfe Identity and function of gamma-secretase J. Neurosci. Res. 74 2003 353 360
39. B. Kostyszyn, R.F. Cowburn, A. Seiger, A. Kjaeldgaard, and E. Sundstrom Distribution of presenilin 1 and 2 and their relation to Notch receptors and ligands in human embryonic/foetal central nervous system Brain Res., Dev. Brain Res. 151 2004 75 86
40. M.J. LaVoie, and D.J. Selkoe The Notch ligands, Jagged and Delta, are sequentially processed by alpha-secretase and presenilin/gamma-secretase and release signaling fragments J. Biol. Chem. 278 2003 34427 34437
41. P.G. Layer, R. Alber, P. Mansky, G. Vollmer, and E. Willbold Regeneration of a chimeric retina from single cells in vitro: cell-lineage-dependent formation of radial cell columns by segregated chick and quail cells Cell Tissue Res. 259 1990 187 198
42. P.G. Layer, A. Robitzki, A. Rothermel, and E. Willbold Of layers and spheres: the reaggregate approach in tissue engineering Trends Neurosci. 25 2002 131 134
43. J. Lewis Neurogenic genes and vertebrate neurogenesis Curr. Opin. Neurobiol. 6 1996 3 10
44. F.J. Livesey, and C.L. Cepko Vertebrate neural cell-fate determination: lessons from the retina Nat. Rev., Neurosci. 2 2001 109 118
45. J. Malicki Development of the retina Methods Cell Biol. 59 1999 273 299
46. J. Malicki, H. Jo, and Z. Pujic Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning Dev. Biol. 259 2003 95 108
47. R.C. Marcus, and S.S. Easter Jr. Expression of glial fibrillary acidic protein and its relation to tract formation in embryonic zebrafish (Danio rerio) J. Comp. Neurol. 359 1995 365 381
48. R.C. Marcus, C.L. Delaney, and S.S. Easter Jr. Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio) Vis. Neurosci. 16 1999 417 424
49. M. Matsunaga, K. Hatta, and M. Takeichi Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina Neuron 1 1988 289 295
50. M.P. Mattson A multi-talented secreted protein Trends Neurosci. 24 2001 441 442
51. K. Meller, and W. Tetzlaff Scanning electron microscopic studies on the development of the chick retina Cell Tissue Res. 170 1976 145 159
52. S.J. Morrison, S.E. Perez, Z. Qiao, J.M. Verdi, C. Hicks, G. Weinmaster, and D.J. Anderson Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells Cell 101 2000 499 510
53. X. Mu, and W.H. Klein A gene regulatory hierarchy for retinal ganglion cell specification and differentiation Semin. Cell Dev. Biol. 15 2004 115 123
54. C. Nuesslein-Volhard, and R. Dahm Zebrafish: A Practical Approach 2002 Oxford University Press New York
55. M. Perron, and W.A. Harris Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors Cell. Mol. Life Sci. 57 2000 215 223
56. R.E. Peterson, J.M. Fadool, J. McClintock, and P.J. Linser Muller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation J. Comp. Neurol. 429 2001 530 540
57. F.A. Prada, M.M. Magalhaes, A. Coimbra, and J.M. Genis-Galvez Morphological differentiation of the Muller cell: Golgi and electron microscopy study in the chick retina J. Morphol. 201 1989 11 22
58. Z. Pujic, and J. Malicki Retinal pattern and the genetic basis of its formation in zebrafish Semin. Cell Dev. Biol. 15 2004 105 114
59. D.H. Rapaport, and R.I. Dorsky Inductive competence, its significance in retinal cell fate determination and a role for Delta-Notch signaling Semin. Cell Dev. Biol. 9 1998 241 247
60. P.A. Raymond, L.K. Barthel, and G.A. Curran Developmental patterning of rod and cone photoreceptors in embryonic zebrafish J. Comp. Neurol. 359 1995 537 550
61. N. Scheer, A. Groth, S. Hans, and J.A. Campos-Ortega An instructive function for Notch in promoting gliogenesis in the zebrafish retina Development 128 2001 1099 1107
62. A. Schier, S. Neuhauss, M. Harvey, J. Malicki, L. Solnica-Krezel, D. Stainier, F. Zwartkruis, S. Abdelilah, D. Stemple, Z. Rangini, H. Yang, and W. Driever Mutations affecting the development of the embryonic zebrafish brain Development 123 1996 165 178
63. E.A. Schmitt, and J.E. Dowling Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish, Danio rerio J. Comp. Neurol. 371 1996 222 234
64. E.A. Schmitt, and J.E. Dowling Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses J. Comp. Neurol. 404 1999 515 536
65. M.L. Schneider, D.L. Turner, and M.L. Vetter Notch signaling can inhibit Xath5 function in the neural plate and developing retina Mol. Cell. Neurosci. 18 2001 458 472
66. B. Schwaller, P. Buchwald, I. Blumcke, M.R. Celio, and W. Hunziker Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin Cell Calcium 14 1993 639 648
67. D. Seiffert, J.D. Bradley, C.M. Rominger, D.H. Rominger, F. Yang, J.E. Meredith Jr., Q. Wang, A.H. Roach, L.A. Thompson, S.M. Spitz, J.N. Higaki, S.R. Prakash, A.P. Combs, R.A. Copeland, S.P. Arneric, P.R. Hartig, D.W. Robertson, B. Cordell, A.M. Stern, R.E. Olson, and R. Zaczek Presenilin-1 and -2 are molecular targets for gamma-secretase inhibitors J. Biol. Chem. 275 2000 34086 34091
68. 3 G.K. Smelser The Structure of the Eye 1961 Academic Press New York 487 505
69. A.O. Silva, C.E. Ercole, and S.C. McLoon Regulation of ganglion cell production by Notch signaling during retinal development J. Neurobiol. 54 2003 511 524
70. H. Steiner, K. Duff, A. Capell, H. Romig, M.G. Grim, S. Lincoln, J. Hardy, X. Yu, M. Picciano, K. Fechteler, M. Citron, R. Kopan, B. Pesold, S. Keck, M. Baader, T. Tomita, T. Iwatsubo, R. Baumeister, and C. Haass A loss of function mutation of Presenilin-2 interferes with amyloid beta-peptide production and Notch signaling J. Biol. Chem. 274 1999 28669 28673
71. D.L. Stenkamp, O. Hisatomi, L.K. Barthel, F. Tokunaga, and P.A. Raymond Temporal expression of rod and cone opsins in embryonic goldfish retina predicts the spatial organization of the cone mosaic Invest. Ophthalmol. Visual Sci. 37 1996 363 376
72. K. Takatsuka, J. Hatakeyama, Y. Bessho, and R. Kageyama Roles of the bHLH gene Hes1 in retinal morphogenesis Brain Res. 1004 2004 148 155
73. C. Takke, P. Dornseifer, E. v Weizsacker, and J.A. Campos-Ortega her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling Development 126 1999 1811 1821
74. D.L. Turner, and C.L. Cepko A common progenitor for neurons and glia persists in rat retina late in development Nature 328 1987 131 136
75. S. Uga, and G.K. Smelser Electron microscopic study of the development of retinal Mullerian cells Invest. Ophthalmol. 12 1973 295 307
76. Z.M. Varga, J. Wegner, and M. Westerfield Anterior movement of ventral diencephalic precursors separates the primordial eye field in the neural plate and requires cyclops Development 126 1999 5533 5546
77. M. Westerfield The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2000 Univ. of Oregon Press Eugene
78. E. Willbold, and P.G. Layer Muller glia cells and their possible roles during retina differentiation in vivo and in vitro Histol. Histopathol. 13 1998 531 552
79. E. Willbold, A. Rothermel, S. Tomlinson, and P.G. Layer Muller glia cells reorganize reaggregating chicken retinal cells into correctly laminated in vitro retinae Glia 29 2000 45 57
80. K. Woo, and S.E. Fraser Order and coherence in the fate map of the zebrafish nervous system Development 121 1995 2595 2609
81. S. Yazulla, and K.M. Studholme Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry J. Neurocytol. 30 2001 551 592
82. R.W. Young Cell differentiation in the retina of the mouse Anat. Rec. 212 1985 199 205