Effects of follistatin overexpression on cell differentiation in the chick embryo retina

Developmental Biology

Volumn 298, Issue 1, 2006, Pages 272-284

  Moreira, Ernesto F ^a   Adler, Ruben ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Apoptosis; Development; Follistatin; Growth factors; Retina; Retrovirus; Transcription factors

Indexed keywords

ACTIVIN; ALKALINE PHOSPHATASE; FOLLISTATIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR CHX10; TRANSCRIPTION FACTOR NEUROM; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DEATH; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO CELL; EYE DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CELL; RETINA HORIZONTAL NERVE CELL; RETROVIRUS; TRANSCRIPTION REGULATION;

SPONDIAS PURPUREA;

EID: 33748759829     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.06.035     Document Type: Article

References (81)

1. Adler R. A model of retinal cell differentiation in the chick embryo. Prog. Retinal Res. 20 (2000) 529-557
2. Adler R., and Belecky-Adams T.L. The role of bone morphogenetic proteins in the differentiation of the ventral optic cup. Development 129 (2002) 3161-3171
3. Adler R., and Hatlee M. Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 243 (1989) 391-393
4. Altmann C.R., and Brivanlou A.H. Neural patterning in the vertebrate embryo. Int. Rev. Cytol. 203 (2001) 447-482
5. Balemans W., and Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250 (2002) 231-250
6. Belecky-Adams T., and Adler R. Developmental expression patterns of bone morphogenetic proteins, receptors, and binding proteins in the chick retina. J. Comp. Neurol. 430 (2001) 562-572
7. Belecky-Adams T., Cook B., and Adler R. Correlations between terminal mitosis and differentiated fate of retinal precursor cells in vivo and in vitro: analysis with the "window-labeling" technique. Dev. Biol. 178 (1996) 304-315
8. Belecky-Adams T., Tomarev S., Li H.S., Ploder L., McInnes R.R., Sundin O., and Adler R. Pax-6, Prox 1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest. Ophthalmol. Visual Sci. 38 (1997) 1293-1303
9. Belecky-Adams T.L., Scheurer D., and Adler R. Activin family members in the developing chick retina: expression patterns, protein distribution, and in vitro effects. Dev. Biol. 210 (1999) 107-123
10. Bertrand N., Castro D.S., and Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev., Neurosci. 3 (2002) 517-530
11. Bovolenta P., Mallamaci A., Briata P., Corte G., and Boncinelli E. Implication of OTX2 in pigment epithelium determination and neural retina differentiation. J. Neurosci. 17 (1997) 4243-4252
12. Bradford R.L., Wang C., Zack D.J., and Adler R. Roles of cell-intrinsic and microenvironmental factors in photoreceptor cell differentiation. Dev. Biol. 286 (2005) 31-45
13. Brown N.L., Patel S., Brzezinski J., and Glaser T. Math5 is required for retinal ganglion cell and optic nerve formation. Development 128 (2001) 2497-2508
14. Burmeister M., Novak J., Liang M.Y., Basu S., Ploder L., Hawes N.L., Vidgen D., Hoover F., Goldman D., Kalnins V.I., Roderick T.H., Taylor B.A., Hankin M.H., and McInnes R.R. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat. Genet. 12 (1996) 376-384
15. Chen C.M., and Cepko C.L. Expression of Chx10 and Chx10-1 in the developing chicken retina. Mech. Dev. 90 (2000) 293-297
16. Chen S., Wang Q.L., Nie Z., Sun H., Lennon G., Copeland N.G., Gilbert D.J., Jenkins N.A., and Zack D.J. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19 (1997) 1017-1030
17. Cook R.W., Thompson T.B., Jardetzky T.S., and Woodruff T.K. Molecular biology of inhibin action. Semin Reprod. Med. 22 (2004) 269-276
18. Davis A.A., Matzuk M.M., and Reh T.A. Activin A promotes progenitor differentiation into photoreceptors in rodent retina. Mol. Cell. Neurosci. 15 (2000) 11-21
19. Drenhaus U., Morino P., and Veh R.W. On the development of the stratification of the inner plexiform layer in the chick retina. J. Comp. Neurol. 460 (2003) 1-12
20. Dyer M.A. Regulation of proliferation, cell fate specification and differentiation by the homeodomain proteins Prox1, Six3, and Chx10 in the developing retina. Cell Cycle 2 (2003) 350-357
21. Dyer M.A., Livesey F.J., Cepko C.L., and Oliver G. Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat. Genet. 34 (2003) 53-58
22. Edqvist P.H., and Hallbook F. Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development. Development 131 (2004) 1343-1351
23. Ellis J.H., Richards D.E., and Rogers J.H. Calretinin and calbindin in the retina of the developing chick. Cell Tissue Res. 264 (1991) 197-208
24. Fischer A.J., Seltner R.L., Poon J., and Stell W.K. Immunocytochemical characterization of quisqualic acid- and N-methyl-d-aspartate-induced excitotoxicity in the retina of chicks. J. Comp. Neurol. 393 (1998) 1-15
25. Fischer A.J., Wallman J., Mertz J.R., and Stell W.K. Localization of retinoid binding proteins, retinoid receptors, and retinaldehyde dehydrogenase in the chick eye. J. Neurocytol. 28 (1999) 597-609
26. Fuhrmann S., Kirsch M., and Hofmann H.D. Ciliary neurotrophic factor promotes chick photoreceptor development in vitro. Development 121 (1995) 2695-2706
27. Fuhrmann S., Heller S., Rohrer H., and Hofmann H.D. A transient role for ciliary neurotrophic factor in chick photoreceptor development. J. Neurobiol. 37 (1998) 672-683
28. Furukawa T., Morrow E.M., and Cepko C.L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91 (1997) 531-541
29. Goureau O., Rhee K.D., and Yang X.J. Ciliary neurotrophic factor promotes Müller glia differentiation from the postnatal retinal progenitor pool. Dev. Neurosci. 26 (2004) 359-370
30. Hamburger V., and Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951) 49-92
31. Harrison C.A., Gray P.C., Vale W.W., and Robertson D.M. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol. Metab. 16 (2005) 73-78
32. Hatakeyama J., Tomita K., Inoue T., and Kageyama R. Roles of homeobox and bHLH genes in specification of a retinal cell type. Development 128 (2001) 1313-1322
33. Hemmati-Brivanlou A., Kelly O.G., and Melton D.A. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77 (1994) 283-295
34. Holt C.E., Bertsch T.W., Ellis H.M., and Harris W.A. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1 (1988) 15-26
35. Hughes S.H., Greenhouse J.J., Petropoulos C.J., and Sutrave P. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61 (1987) 3004-3012
36. Iemura S., Yamamoto T.S., Takagi C., Uchiyama H., Natsume T., Shimasaki S., Sugino H., and Ueno N. Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9337-9342
37. Inoue T., Hojo M., Bessho Y., Tano Y., Lee J.E., and Kageyama R. Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129 (2002) 831-842
38. Kim J., Wu H.H., Lander A.D., Lyons K.M., Matzuk M.M., and Calof A.L. GDF11 controls the timing of progenitor cell competence in developing retina. Science 308 (2005) 1927-1930
39. Kubo F., Takeichi M., and Nakagawa S. Wnt2b controls retinal cell differentiation at the ciliary marginal zone. Development 130 (2003) 587-598
40. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122 (2005) 3-25
41. Levin M., Johnson R.L., Stern C.D., Kuehn M., and Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82 (1995) 803-814
42. Liu W., Khare S.L., Liang X., Peters M.A., Liu X., Cepko C.L., and Xiang M. All Brn3 genes can promote retinal ganglion cell differentiation in the chick. Development 127 (2000) 3237-3247
43. Liu W., Mo Z., and 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. U. S. A. 98 (2001) 1649-1654
44. Liu H., Mohamed O., Dufort D., and Wallace V.A. Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina. Dev. Dyn. 227 (2003) 323-334
45. Ma W., Yan R.T., Xie W., and Wang S.Z. A role of ath5 in inducing neuroD and the photoreceptor pathway. J. Neurosci. 24 (2004) 7150-7158
46. MacNeil M.A., and Masland R.H. Extreme diversity among amacrine cells: implications for function. Neuron 20 (1998) 971-982
47. Malicki J. Cell fate decisions and patterning in the vertebrate retina: the importance of timing, asymmetry, polarity and waves. Curr. Opin. Neurobiol. 14 (2004) 15-21
48. Marquardt T., Ashery-Padan R., Andrejewski N., Scardigli R., Guillemot F., and Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105 (2001) 43-55
49. Masai I., Stemple D.L., Okamoto H., and Wilson S.W. Midline signals regulate retinal neurogenesis in zebrafish. Neuron 27 (2000) 251-263
50. Matter-Sadzinski L., Matter J.M., Ong M.T., Hernandez J., and Ballivet M. Specification of neurotransmitter receptor identity in developing retina: the chick ATH5 promoter integrates the positive and negative effects of several bHLH proteins. Development 128 (2001) 217-231
51. McLoon S.C., and Barnes R.B. Early differentiation of retinal ganglion cells: an axonal protein expressed by premigratory and migrating retinal ganglion cells. J. Neurosci. 9 (1989) 1424-1432
52. Mears A.J., Kondo M., Swain P.K., Takada Y., Bush R.A., Saunders T.L., Sieving P.A., and Swaroop A. Nrl is required for rod photoreceptor development. Nat. Genet. 29 (2001) 447-452
53. Moreira E.F., Jaworski C., Li A., and Rodriguez I.R. Molecular and biochemical characterization of a novel oxysterol-binding protein (OSBP2) highly expressed in retina. J. Biol. Chem. 276 (2001) 18570-18578
54. Morgan B.A., and Fekete D.M. Manipulating gene expression with replication-competent retroviruses. Methods Cell Biol. 51 (1996) 185-218
55. Mu X., Fu X., Sun H., Beremand P.D., Thomas T.L., and Klein W.H. A gene network downstream of transcription factor Math5 regulates retinal progenitor cell competence and ganglion cell fate. Dev. Biol. 280 (2005) 467-481
56. Murali D., Yoshikawa S., Corrigan R.R., Plas D.J., Crair M.C., Oliver G., Lyons K.M., Mishina Y., and Furuta Y. Distinct developmental programs require different levels of BMP signaling during mouse retinal development. Development 132 (2005) 913-923
57. Murphy D.B. Fundamentals of Light Microscopy (2001), Wiley-Liss, Inc., New York
58. North A.J. Seeing is believing? A beginners' guide to practical pitfalls in image acquisition. J. Cell Biol. 172 (2006) 9-18
59. Pittack C., Grunwald G.B., and Reh T.A. Fibroblast growth factors are necessary for neural retina but not pigmented epithelium differentiation in chick embryos. Development 124 (1997) 805-816
60. Pituello F., Yamada G., and Gruss P. Activin A inhibits Pax-6 expression and perturbs cell differentiation in the developing spinal cord in vitro. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 6952-6956
61. Portera-Cailliau C., Sung C.H., Nathans J., and Adler R. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 974-978
62. Prada C., Puga J., Perez-Mendez L., Lopez R., and Ramirez G. Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 3 (1991) 559-569
63. Prada F., Medina J.I., Lopez-Gallardo M., Lopez R., Quesada A., Spira A., and Prada C. Spatiotemporal gradients of differentiation of chick retina types I and II cholinergic cells: identification of a common postmitotic cell population. J. Comp. Neurol. 410 (1999) 457-466
64. Roztocil T., Matter-Sadzinski L., Alliod C., Ballivet M., and Matter J.M. NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neurogenesis. Development 124 (1997) 3263-3272
65. Selleck M.A.J. Culture and microsurgical manipulation of the early avian embryo. In: Bronner-Frasier M. (Ed). Methods in Cell Biology vol. 51 (1996), Academic Press, Inc., San Diego 1-21
66. Thompson T.B., Lerch T.F., Cook R.W., Woodruff T.K., and Jardetzky T.S. The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 9 (2005) 535-543
67. Timmer J., Chesnutt C., and Niswander L. The activin signaling pathway promotes differentiation of dI3 interneurons in the spinal neural tube. Dev. Biol. 285 (2005) 1-10
68. Tomarev S.I., Sundin O., Banerjee-Basu S., Duncan M.K., Yang J.M., and Piatigorsky J. Chicken homeobox gene Prox 1 related to Drosophila prospero is expressed in the developing lens and retina. Dev. Dyn. 206 (1996) 354-367
69. Tomita K., Ishibashi M., Nakahara K., Ang S.L., Nakanishi S., Guillemot F., and Kageyama R. Mammalian hairy and enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16 (1996) 723-734
70. Tomita K., Nakanishi S., Guillemot F., and Kageyama R. Mash1 promotes neuronal differentiation in the retina. Genes Cells 1 (1996) 765-774
71. Turner D.L., and Cepko C.L. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328 (1987) 131-136
72. Van Raay T.J., and Vetter M.L. Wnt/frizzled signaling during vertebrate retinal development. Dev. Neurosci. 26 (2004) 352-358
73. Wahlin K.J., Lim L., Grice E.A., Campochiaro P.A., Zack D.J., and Adler R. A method for analysis of gene expression in isolated mouse photoreceptor and Müller cells. Mol. Vision 10 (2004) 366-375
74. Wang Y.P., Dakubo G., Howley P., Campsall K.D., Mazarolle C.J., Shiga S.A., Lewis P.M., McMahon A.P., and Wallace V.A. Development of normal retinal organization depends on Sonic hedgehog signaling from ganglion cells. Nat. Neurosci. 5 (2002) 831-832
75. Wetts R., and Fraser S.E. Multipotent precursors can give rise to all major cell types of the frog retina. Science 239 (1988) 1142-1145
76. Wilson P.A., and Hemmati-Brivanlou A. Vertebrate neural induction: inducers, inhibitors, and a new synthesis. Neuron 18 (1997) 699-710
77. Xie H.Q., and Adler R. Green cone opsin and rhodopsin regulation by CNTF and staurosporine in cultured chick photoreceptors. Invest. Ophthalmol. Visual Sci. 41 (2000) 4317-4323
78. Yamagata M., Weiner J.A., and Sanes J.R. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110 (2002) 649-660
79. Yan R.T., and Wang S.Z. Requirement of neuroD for photoreceptor formation in the chick retina. Invest. Ophthalmol. Visual Sci. 45 (2004) 48-58
80. Yang X.J. Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol. 15 (2004) 91-103
81. Zhang X.M., and Yang X.J. Regulation of retinal ganglion cell production by Sonic hedgehog. Development 128 (2001) 943-957