Basic fibroblast growth factor increases the precursor pool of photoreceptors, but inhibits their differentiation and apoptosis in chicken retinal reaggregates

European Journal of Neuroscience

Volumn 29, Issue 10, 2009, Pages 1931-1942

  Frohns, Florian ^a   Mager, Magnus ^b   Layer, Paul G ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b CERN   (Switzerland)

Author keywords

Cones; Cytokines; Retinal spheroids; Rods; Three dimensional cell culture

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CELL ANTIBODY; DNA NUCLEOTIDYLEXOTRANSFERASE; FIBROBLAST GROWTH FACTOR 2; SURAMIN;

ANIMAL CELL; ANTIGEN BINDING; APOPTOSIS; ARTICLE; CELL AGING; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL PROTECTION; CELL SIZE; CELL SUBPOPULATION; CELL SURVIVAL; CHICKEN; CONTROLLED STUDY; EMBRYO; IMMUNOCHEMISTRY; NICK END LABELING; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BLOCKING; RETINA; RETINA AMACRINE CELL; RETINA CONE; RETINA ROD; SIGNAL TRANSDUCTION; SPHEROID CELL; STEM CELL;

ANIMALS; APOPTOSIS; CELL AGGREGATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; FIBROBLAST GROWTH FACTOR 2; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; PHOTORECEPTOR CELLS; SPHEROIDS, CELLULAR;

EID: 65749089202     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06738.x     Document Type: Article

References (43)

1. Adler, R. Raymond, P.A. (2008) Have we achieved a unified model of photoreceptor cell fate specification in vertebrates? Brain Res., 1192, 34 50.
2. Botta, M., Manetti, F. Corelli, F. (2000) Fibroblast growth factors and their inhibitors. Curr. Pharm. Des., 6, 1897 1924.
3. Bruhn, S.L. Cepko, C.L. (1996) Development of the pattern of photoreceptors in the chick retina. J. Neurosci., 16, 1430 1439. (Pubitemid 26145923)
4. Cirillo, A., Chifflet, S. Villar, B. (2001) Neural retina of chick embryo in organ culture: effects of blockade of growth factors by suramin. Cell Tissue Res., 304, 323 331. (Pubitemid 32480562)
5. Consigli, S.A., Lyser, K.M. Joseph-Silverstein, J. (1993) The temporal and spatial expression of basic fibroblast growth factor during ocular development in the chicken. Invest. Ophthalmol. Vis. Sci., 34, 559 566. (Pubitemid 23095209)
6. Desire, L., Courtois, Y. Jeanny, J.C. (1998) Suppression of fibroblast growth factors 1 and 2 by antisense oligonucleotides in embryonic chick retinal cells in vitro inhibits neuronal differentiation and survival. Exp. Cell Res., 241, 210 221. (Pubitemid 28366596)
7. Desire, L., Courtois, Y. Jeanny, J.C. (2000) Endogenous and exogenous fibroblast growth factor 2 support survival of chick retinal neurons by control of neuronal neuronal bcl-x(L) and bcl-2 expression through a fibroblast growth factor receptor 1- and ERK-dependent pathway. J. Neurochem., 75, 151 163. (Pubitemid 30418180)
8. Ezeonu, I., Derrickson, B. Dutt, K. (2000) Cell fate decisions in a human retinal precursor cell line: basic fibroblast growth factor- and transforming growth factor-alpha-mediated differentiation. DNA Cell Biol., 19, 527 537.
9. Fischer, A.J. Omar, G. (2005) Transitin, a nestin-related intermediate filament, is expressed by neural progenitors and can be induced in Muller glia in the chicken retina. J. Comp. Neurol., 484, 1 14. (Pubitemid 40315401)
10. Fischer, A.J., Dierks, B.D. Reh, T.A. (2002a) Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development, 129, 2283 2291.
11. Fischer, A.J., McGuire, C.R., Dierks, B.D. Reh, T.A. (2002b) Insulin and fibroblast growth factor 2 activate a neurogenic program in Muller glia of the chicken retina. J. Neurosci., 22, 9387 9398. (Pubitemid 35356182)
12. Fischer, A.J., Foster, S., Scott, M.A. Sherwood, P. (2008) Transient expression of LIM-domain transcription factors is coincident with delayed maturation of photoreceptors in the chicken retina. J. Comp. Neurol., 506, 584 603.
13. Fontaine, V., Kinkl, N., Sahel, J., Dreyfus, H. Hicks, D. (1998) Survival of purified rat photoreceptors in vitro is stimulated directly by fibroblast growth factor-2. J. Neurosci., 18, 9662 9672. (Pubitemid 28543747)
14. Ghai, K., Stanke, J.J. Fischer, A.J. (2008) Patterning of the circumferential marginal zone of progenitors in the chicken retina. Brain Res., 1192, 76 89.
15. Harris, W.A. Messersmith, S.L. (1992) Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron, 9, 357 372.
16. Haynes, T., Gutierrez, C., Aycinena, J.C., Tsonis, P.A. Del Rio-Tsonis, K. (2007) BMP signaling mediates stem/progenitor cell-induced retina regeneration. Proc. Natl Acad. Sci. USA, 104, 20380 20385.
17. Hicks, D. (1996) Characterization and possible roles of fibroblast growth factors in retinal photoreceptor cells. Keio J. Med., 45, 140 154. (Pubitemid 126557323)
18. Hicks, D., Heidinger, V., Mohand-Said, S., Sahel, J. Dreyfus, H. (1998) Growth factors and gangliosides as neuroprotective agents in excitotoxicity and ischemia. Gen. Pharmacol., 30, 265 273. (Pubitemid 28046494)
19. Jacob, V., Rothermel, A., Wolf, P. Layer, P.G. (2005) Rhodopsin, violet and blue opsin expressions in the chick are highly dependent on tissue and serum conditions. Cells Tissues Organs, 180, 159 168. (Pubitemid 41547098)
20. Kahn, A.J. (1974) An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev. Biol., 38, 30 40.
21. Karim, S.A. de Pomerai, D.I. (1990) Stimulatory effects of retinal extract and fibroblast growth factor on lentoidogenesis in cultures of chick embryo neuroretinal cells. Cell Differ. Dev., 31, 169 176. (Pubitemid 20304735)
22. Kathir, K.M., Kumar, T.K. Yu, C. (2006) Understanding the mechanism of the antimitogenic activity of suramin. Biochemistry, 45, 899 906. (Pubitemid 43122254)
23. Layer, P.G., Rothermel, A. Willbold, E. (2001) From stem cells towards neural layers: a lesson from re-aggregated embryonic retinal cells. Neuroreport, 12, A39 46. (Pubitemid 32476120)
24. Layer, P.G., Robitzki, A., Rothermel, A. Willbold, E. (2002) Of layers and spheres: the reaggregate approach in tissue engineering. Trends Neurosci., 25, 131 134. (Pubitemid 34164333)
25. Leveillard, T., Mohand-Said, S., Lorentz, O., Hicks, D., Fintz, A.C., Clerin, E., Simonutti, M., Forster, V., Cavusoglu, N., Chalmel, F., Dolle, P., Poch, O., Lambrou, G. Sahel, J.A. (2004) Identification and characterization of rod-derived cone viability factor. Nat. Genet., 36, 755 759. (Pubitemid 38886639)
26. Livesey, F.J. Cepko, C.L. (2001) Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci., 2, 109 118. (Pubitemid 33673365)
27. Mao, J., Liu, S., Wen, D., Tan, X. Fu, C. (2006) Basic fibroblast growth factor suppresses retinal neuronal apoptosis in form-deprivation myopia in chicks. Curr. Eye Res., 31, 983 987.
28. Mey, J. Thanos, S. (2000) Development of the visual system of the chick. I. Cell differentiation and histogenesis. Brain Res. Brain Res. Rev., 32, 343 379. (Pubitemid 30171313)
29. O'Driscoll, C., O'Connor, J., O'Brien, C.J. Cotter, T.G. (2008) Basic fibroblast growth factor-induced protection from light damage in the mouse retina in vivo. J. Neurochem., 105, 524 536.
30. Prada, C., Puga, J., Perez-Mendez, L., Lopez, R. Ramirez, G. (1991) Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci., 3, 559 569.
31. Rothermel, A. Layer, P.G. (2001) Photoreceptor plasticity in reaggregates of embryonic chick retina: rods depend on proximal cones and on tissue organization. Eur. J. Neurosci., 13, 949 958. (Pubitemid 32226146)
32. Rothermel, A. Layer, P.G. (2003) GDNF regulates chicken rod photoreceptor development and survival in reaggregated histotypic retinal spheres. Invest. Ophthalmol. Vis. Sci., 44, 2221 2228. (Pubitemid 36520320)
33. Rothermel, A., Willbold, E., DeGrip, W.J. Layer, P.G. (1997) Pigmented epithelium induces complete retinal reconstitution from fully dispersed embryonic chick retinae in reaggregation culture. Proc. R. Soc. Lond. Ser. B, 264, 1293 1302. (Pubitemid 27445227)
34. Rothermel, A., Volpert, K., Burghardt, M., Lantzsch, C., Robitzki, A.A. Layer, P.G. (2006) Knock-down of GFRalpha4 expression by RNA interference affects the development of retinal cell types in three-dimensional histiotypic retinal spheres. Invest. Ophthalmol. Vis. Sci., 47, 2716 2725.
35. Sakaguchi, D.S., Janick, L.M. Reh, T.A. (1997) Basic fibroblast growth factor (FGF-2) induced transdifferentiation of retinal pigment epithelium: generation of retinal neurons and glia. Dev. Dyn., 209, 387 398. (Pubitemid 27328465)
36. Tcheng, M., Oliver, L., Courtois, Y. Jeanny, J.C. (1994) Effects of exogenous FGFs on growth, differentiation, and survival of chick neural retina cells. Exp. Cell Res., 212, 30 35. (Pubitemid 24167354)
37. Vollmer, G. Layer, P.G. (1986) An in vitro model of proliferation and differentiation of the chick retina: coaggregates of retinal and pigment epithelial cells. J. Neurosci., 6, 1885 1896. (Pubitemid 16064952)
38. Volpert, K.N., Rothermel, A. Layer, P.G. (2007) GDNF stimulates rod photoreceptors and dopaminergic amacrine cells in chicken retinal reaggregates. Invest. Ophthalmol. Vis. Sci., 48, 5306 5314.
39. Wohabrebbi, A., Umstot, E.S., Iannaccone, A., Desiderio, D.M. Jablonski, M.M. (2002) Downregulation of a unique photoreceptor protein correlates with improper outer segment assembly. J. Neurosci. Res., 67, 298 308. (Pubitemid 34137136)
40. Yamagata, K., Goto, K., Kuo, C.H., Kondo, H. Miki, N. (1990) Visinin: a novel calcium binding protein expressed in retinal cone cells. Neuron, 4, 469 476. (Pubitemid 20155037)
41. Yan, R.T. Wang, S.Z. (2000) Differential induction of gene expression by basic fibroblast growth factor and neuroD in cultured retinal pigment epithelial cells. Vis. Neurosci., 17, 157 164. (Pubitemid 30241018)
42. Yang, X.J. (2004) Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol., 15, 91 103. (Pubitemid 38177373)
43. Zinchuk, V., Zinchuk, O. Okada, T. (2007) Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem. Cytochem., 40, 101 111. (Pubitemid 47416687)