Secreted inducers in vertebrate eye development: More functions for old morphogens

Current Opinion in Neurobiology

Volumn 16, Issue 1, 2006, Pages 13-19

  Esteve, Pilar ^a   Bovolenta, Paola ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; MORPHOGEN; WNT PROTEIN;

CELL COUNT; CELL SPECIFICITY; CELL TYPE; CELLULAR DISTRIBUTION; EMBRYONAL TISSUE; EYE DEVELOPMENT; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; RETINA NERVE CELL; REVIEW; SCIENCE; SIGNAL TRANSDUCTION; VERTEBRATE; VISUAL FIELD;

ANIMALS; EYE; FIBROBLAST GROWTH FACTORS; MORPHOGENESIS; SIGNAL TRANSDUCTION; VERTEBRATES; VISUAL FIELDS;

EID: 32344435631     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2006.01.001     Document Type: Review

References (50)

1. X.J. Yang Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis Semin Cell Dev Biol 15 2004 91 103
2. J.R. Martinez-Morales, I. Rodrigo, and P. Bovolenta Eye development: a view from the pigmented epithelium Bioessays 26 2004 766 777
3. P. Bovolenta Morphogen signaling at the vertebrate growth cone: a few cases or a general strategy? J Neurobiol 64 2005 405 416
4. G. Eagleson, B. Ferreiro, and W.A. Harris Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain J Neurobiol 28 1995 146 158
5. 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
6. T. Inoue, S. Nakamura, and N. Osumi Fate mapping of the mouse prosencephalic neural plate Dev Biol 219 2000 373 383
7. P. Fernandez-Garre, L. Rodriguez-Gallardo, V. Gallego-Diaz, I.S. Alvarez, and L. Puelles Fate map of the chicken neural plate at stage 4 Development 129 2002 2807 2822
8. R. Wetts, and S.E. Fraser Slow intermixing of cells during Xenopus embryogenesis contributes to the consistency of the blastomere fate map Development 105 1989 9 15
9. Y. Hirose, Z.M. Varga, H. Kondoh, and M. Furutani-Seiki Single cell lineage and regionalization of cell populations during Medaka neuralation Development 131 2004 2553 2563
10. J.C. Chuang, and P.A. Raymond Embryonic origin of the eyes in teleost fish Bioessays 24 2002 519 529
11. K.L. Kenyon, N. Zaghloul, and S.A. Moody Transcription factors of the anterior neural plate alter cell movements of epidermal progenitors to specify a retinal fate Dev Biol 240 2001 77 91
12. K.B. Moore, K. Mood, I.O. Daar, and S.A. Moody Morphogenetic movements underlying eye field formation require interactions between the FGF and ephrinB1 signaling pathways Dev Cell 6 2004 55 67 During formation of the anterior neural ectoderm, cells that will form the different forebrain regions are randomly dispersed and need to move into the correct position to be induced to express tissue-specific genes. The authors demonstrate here that in Xenopus embryos, this positioning is promoted by the interaction of FGF and ephrin signaling pathways.
13. D.G. Wilkinson Multiple roles of EPH receptors and ephrins in neural development Nat Rev Neurosci 2 2001 155 164
14. L.D. Chong, E.K. Park, E. Latimer, R. Friesel, and I.O. Daar Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos Mol Cell Biol 20 2000 724 734
15. L. Solnica-Krezel Conserved patterns of cell movements during vertebrate gastrulation Curr Biol 15 2005 R213 R228
16. F. Cavodeassi, F. Carreira-Barbosa, R.M. Young, M.L. Concha, M.L. Allende, C. Houart, M. Tada, and S.W. Wilson Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway Neuron 47 2005 43 56 Wnt signaling contributes to the early subregionalisation of the anterior neural plate, but its role in the specification of eye field progenitors is unclear. Using cell transplants to alter different components of both canonical and non-canonical Wnt signaling locally, the authors demonstrate that both branches of the pathway contribute to eye formation. Wnt8- Fz8-mediated activation of Wnt/βcatenin signaling inhibits eye formation, whereas Wnt11- Fz5-mediated local activation of non-canonical signaling favors eye development with a dual function: promoting the cohesion of the eye field cells and inhibiting the Wnt/βcatenin pathway. This is a clear demonstration that non-canonical Wnt signaling contributes to early eye formation.
17. S.W. Wilson, and C. Houart Early steps in the development of the forebrain Dev Cell 6 2004 167 181 This is a very useful comprehensive and critical overview of the early events in forebrain development.
18. J.B. Gurdon, and P.Y. Bourillot Morphogen gradient interpretation Nature 413 2001 797 803
19. Y. Kawano, and R. Kypta Secreted antagonists of the Wnt signaling pathway J Cell Sci 116 2003 2627 2634
20. C. Houart, L. Caneparo, C. Heisenberg, K. Barth, M. Take-Uchi, and S.W. Wilson Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling Neuron 35 2002 255 265
21. P. Esteve, J. Lopez-Ríos, and P. Bovolenta SFRP1 is required for the proper establishment of the eye field in the medaka fish Mech Dev 121 2004 687 701 Members of the secreted frizzled related protein family, a class of Wnt inhibitors, are expressed in the anterior neural plate. Their expression might help to maintain a posterior-high, anterior-low gradient of Wnt/βcatenin activity, which should contribute to specify anterior neural plate cells in presumptive diencephalon, eye and telencephalon. In contrast to what is predicted by this model, knockdown of Sfrp1 reduces the eye-field size and expands the presumptive telencephalic territory. To explain this result, the authors propose that Sfrp1 functions by modulating non-canonical Wnt signaling.
22. S.H. Kim, J. Shin, H.C. Park, S.Y. Yeo, S.K. Hong, S. Han, M. Rhee, C.H. Kim, A.B. Chitnis, and T.L. Huh Specification of an anterior neuroectoderm patterning by Frizzled8a-mediated Wnt8b signaling during late gastrulation in zebrafish Development 129 2002 4443 4455
23. C.P. Heisenberg, C. Houart, M. Take-Uchi, G.J. Rauch, N. Young, P. Coutinho, I. Masai, L. Caneparo, M.L. Concha, and R. Geisler A mutation in the Gsk3-binding domain of zebrafish Masterblind/Axin1 leads to a fate transformation of telencephalon and eyes to diencephalon Genes Dev 15 2001 1427 1434
24. J.T. Rasmussen, M.A. Deardorff, C. Tan, M.S. Rao, P.S. Klein, and M.L. Vetter Regulation of eye development by frizzled signaling in Xenopus Proc Natl Acad Sci USA 98 2001 3861 3866
25. D. Maurus, C. Heligon, A. Burger-Schwarzler, A.W. Brandli, and M. Kuhl Noncanonical Wnt-4 signaling and EAF2 are required for eye development in Xenopus laevis EMBO J 24 2005 1181 1191
26. •].
27. T. Yabe, T. Shimizu, O. Muraoka, Y.K. Bae, T. Hirata, H. Nojima, A. Kawakami, T. Hirano, and M. Hibi Ogon/Secreted Frizzled functions as a negative feedback regulator of Bmp signaling Development 130 2003 2705 2716
28. S.A. Moody To differentiate or not to differentiate: regulation of cell fate decisions by being in the right place at the right time Cell Cycle 3 2004 564 566
29. Z. Yang, K. Ding, L. Pan, M. Deng, and L. Gan Math5 determines the competence state of retinal ganglion cell progenitors Dev Biol 264 2003 240 254
30. J.N. Kay, B.A. Link, and H. Baier Staggered cell-intrinsic timing of ath5 expression underlies the wave of ganglion cell neurogenesis in the zebrafish retina Development 132 2005 2573 2585 In the retina, neurogenesis spreads in a precise spatio-temporal pattern. It has been proposed that propagation of differentiation is controlled by Shh signaling provided by newly generated RGCs. Here, the authors challenge this model by revealing that a progenitor cell intrinsic-program is sufficient to drive neurogenesis across the zebrafish retina. The authors propose that cell-cell signaling (possibly midline-derived Shh) might be important before the onset of neurogenesis to organize this intrinsic program, thus bringing about retinotopic differences in timing of neurogenesis. This is a provocative and different view of the mechanism that controls RGC differentiation.
31. I. Masai, M. Yamaguchi, N. Tonou-Fujimori, A. Komori, and H. Okamoto 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 132 2005 1539 1553
32. M. Hu, and S.S. Easter Retinal neurogenesis: the formation of the initial central patch of postmitotic cells Dev Biol 207 1999 309 321
33. C.E. Holt, T.W. Bertsch, H.M. Ellis, and W.A. Harris Cellular determination in the Xenopus retina is independent of lineage and birth date Neuron 1 1988 15 26
34. K.L. McCabe, E.C. Gunther, and T.A. Reh The development of the pattern of retinal ganglion cells in the chick retina: mechanisms that control differentiation Development 126 1999 5713 5724
35. J.R. Martinez-Morales, F. Del Bene, G. Nica, M. Hammerschmidt, P. Bovolenta, and J. Wittbrodt Differentiation of the vertebrate retina is coordinated by an FGF signaling center Dev Cell 8 2005 565 574 Previous studies in zebrafish suggested that neurogenesis in the retina is initiated by an unknown midline-dependent signal that is possibly secreted by the distal optic stalk. Using chick and zebrafish embryos, the authors demonstrate a conserved role for Fgf signaling in the initiation of RGC differentiation. The concerted, species-specific localized expression of Fgf8 and Fgf3 is both necessary and sufficient to trigger retinal differentiation. The authors propose that an Fgf signaling center functions as a mediator of the midline signals.
36. I. Masai, D.L. Stemple, H. Okamoto, and S.W. Wilson Midline signals regulate retinal neurogenesis in zebrafish Neuron 27 2000 251 263
37. S. Shanmugalingam, C. Houart, A. Picker, F. Reifers, R. Macdonald, A. Barth, K. Griffin, M. Brand, and S.W. Wilson Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon Development 127 2000 2549 2561
38. W. Herzog, C. Sonntag, S. von der Hardt, H.H. Roehl, Z.M. Varga, and M. Hammerschmidt Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis Development 131 2004 3681 3692
39. N. Powles, H. Marshall, A. Economou, C. Chiang, A. Murakami, C. Dickson, R. Krumlauf, and M. Maconochie Regulatory analysis of the mouse Fgf3 gene: control of embryonic expression patterns and dependence upon sonic hedgehog (Shh) signaling Dev Dyn 230 2004 44 56
40. L. Dailey, D. Ambrosetti, A. Mansukhani, and C. Basilico Mechanisms underlying differential responses to FGF signaling Cytokine Growth Factor Rev 16 2005 233 247
41. C.J. Neumann, and C. Nuesslein-Volhard Patterning of the zebrafish retina by a wave of sonic hedgehog activity Science 289 2000 2137 2139
42. X.M. Zhang, and X.J. Yang Regulation of retinal ganglion cell production by Sonic hedgehog Development 128 2001 943 957
43. D.L. Stenkamp, and R.A. Frey Extraretinal and retinal hedgehog signaling sequentially regulate retinal differentiation in zebrafish Dev Biol 258 2003 349 363
44. X. Mu, X. Fu, H. Sun, S. Liang, H. Maeda, L.J. Frishman, and W.H. Klein Ganglion cells are required for normal progenitor- cell proliferation but not cell-fate determination or patterning in the developing mouse retina Curr Biol 15 2005 525 530 It has been proposed that differentiated neurons of the vertebrate retina influence the properties of progenitor cells but their exact role is still unclear. The authors address this question by analyzing the retinal phenotype of mouse embryos that have their retinal ganglion cells genetically ablated as they are born. They conclude that retinal ganglion cells do not influence cell fate but promote proliferation of progenitor cells. They propose that a secreted signal, probably Shh, mediates this effect.
45. A.M. Kenney, and D.H. Rowitch Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors Mol Cell Biol 20 2000 9055 9056
46. D.K. Waid, and S.C. McLoon Ganglion cells influence the fate of dividing retinal cells in culture Development 125 1998 1059 1066
47. M. Gonzalez-Hoyuela, J.A. Barbas, and A. Rodriguez-Tebar The autoregulation of retinal ganglion cell number Development 128 2001 117 124
48. J. Kim, H.H. Wu, A.D. Lander, K.M. Lyons, M.M. Matzuk, and A.L. Calof GDF11 controls the timing of progenitor cell competence in developing retina Science 308 2005 1927 1930 Previous studies proposed that retinal ganglion cells regulated their own numbers through a feedback mechanism [ 46,47 ]. Analysis of Gdf11 knockout mice reveals that this member of the TGFβ family plays an important role in the control of RGC cell number by regulating the duration of the expression of genes crucial for progenitor cell fate determination. This mechanism is different from that used by GDF11 in the olfactory epithelium. There, neuronal GDF11 controls neurogenesis by regulating progenitor cell proliferation, an interesting twist to the story.
49. Y. Wang, G.D. Dakubo, S. Thurig, C.J. Mazerolle, and V.A. Wallace Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina Development 132 2005 5103 5113 This study describes the effects of the conditional ablation of Shh expression in the peripheral retina of mouse embryos. On the basis of their results the authors propose that in the mouse retina Shh signalling is required to maintain progenitor proliferation and to control the timing of RGC development. These effects are different from those observed in zebrafish where Shh signalling drives cell cycle exit and RGC development [ 31,41,43,50 ]. Species-specific differences in the timing of neurogenesis might be an explanation for this discrepancy.
50. A. Shkumatava, and C.J. Neumann Shh directs cell-cycle exit by activating p57Kip2 in the zebrafish retina EMBO Rep 6 2005 563 569