Suppression of fibroblast growth factor 2 expression by antisense oligonucleotides inhibits embryonic chick neural retina cell differentiation and survival in vivo

Developmental Dynamics

Volumn 212, Issue 1, 1998, Pages 63-74

  Désiré, Laurent ^a   Head, Mark W ^a,b   Fayein, Nicole A ^a,c   Courtois, Yves ^a   Jeanny, Jean Claude ^a,d  

^a BICHAT HOSPITAL   (France)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c CNRS   (France)

^d INSERM   (France)

Author keywords

Antisense oligonucleotide; Chick embryo; Development; Differentiation; Fibroblast growth factor 2; Ganglion cells; Neural retina; Neurotrophic factor; Photoreceptors; Survival

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; FIBROBLAST GROWTH FACTOR 2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CHICK EMBRYO; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION REGULATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA NEUROEPITHELIAL LAYER;

ANIMALS; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL SURVIVAL; CELLS, CULTURED; CHICK EMBRYO; DOWN-REGULATION; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; OLIGONUCLEOTIDES, ANTISENSE; RETINA; RETINAL GANGLION CELLS;

ANIMALIA; AVES; VERTEBRATA;

EID: 0031968147     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199805)212:1<63::AID-AJA6>3.0.CO;2-0     Document Type: Article

References (69)

1. Ahmad I, Dooley CM, Polk DL. Delta-1 is a regulator of neurogenesis in the vertebrate retina. Dev. Biol. 1997;185:92-103.
2. Austin CP, Feldman DE, Ida JA Jr, Cepko CL. Ganglion cells in the vertebrate retina are selected from an equivalence group regulated by Notch. Development 1995;121:3637-3650.
3. Baird A, Klagsbrun M. The fibroblast growth factor family. In: Baird A, Klagsbrun M, eds. The Fibroblast Growth Factor Family. New York: New York Academy of Science, 1991;xi-xii.
4. Belecky-Adams T, Tomarev S, Li HS, Ploder L, McInnes RR, Sundin O, Adler R. Pax-6, Prox-1 and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest. Ophtalmol. Vis. Sci. 1997;38:1293-1303.
5. Benimetskaya L, Tonkinson JL, Koziolkiewicz M, Karwowski B, Guga P, Zeltser R, Stec W, Stein CA. Binding of phosphorothioate oligodeoxynucleotides to basic fibroblast growth factor, recombinant soluble CD4, laminin and fibronectin is P-chirality independent. Nucleic Acids Res. 1995;23:4239-4245.
6. Bennet CF, Chiang MY, Chan H, Shoemaker JE, Mirabelli CK. Cationic lipids enhance cellular uptake and activity of phosphorothioate antisense oligonucleotides. Mol. Pharmacol. 1992;41:1023-1033.
7. Borja ZA, Meijers C, Zeller R. Expression of alternatively spliced bFGF first coding exons and antisense mRNAs during chicken embryogenesis. Dev. Biol. 1993;157:110-118.
8. Bovolenta P, Frade JM, Marti E, Rodriguez-Pena MA, Barde YA, Rodriguez-Tebar A. Neurotrophin-3 antibodies disrupt the normal development of the chick retina. J. Neurosci. 1996;16:4402-4410.
9. Bruhn SL, Cepko CL. Development of the pattern of photoreceptors in the chick retina. J. Neurosci. 1996;16:1430-1439.
10. Burgess WH, Maciag T. The heparin binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem. 1989;58:575-606.
11. Campochiaro PA, Chang M, Ohsato M, Vinores SA, Nie Z, Hjelmeland L, Mansukhani A, Basilico C, Zack DJ. Retinal degeneration in transgenic mice with photoreceptor-specific expression of a dominant-negative fibroblast growth factor receptor. J. Neurosci. 1996;16:1679-1688.
12. Capaccioli S, Di Pasquale G, Mini E, Mazzei T, Quattrone A. Cationic lipids improve antisense oligonucleotide uptake and prevent degradation in cultured cells and in human serum. Biochem. Biophys. Res. Commun. 1993;197:818-825.
13. Chomczynski P, Sacchi N. Single step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987;162:156-159.
14. Clarenc JP, Lebleu B, Léonetti JP. Characterisation of the nuclear binding sites of oligodeoxyribonucleotides and their analogs. J. Biol. Chem. 1993;268:5600-5604.
15. Consigli SA, Lyser KM, Joseph-Silverstein J. The temporal and spatial expression of basic fibroblast growth factor during ocular development in the chicken. Invest. Ophthalmol. Vis. Sci. 1993;34:559-566.
16. Ezzedine ZD, Yang X, DeChiara T, Yancopoulos G, Cepko CL. Postmitotic cells fated to become rods photoreceptors can be respecified by CNTF treatment of the retina. Development 1997;124:1055-1067.
17. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature 1990;347:83-86.
18. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J. Neurosci. 1992;12:3554-3567.
19. Fayein NA, Head MW, Jeanny JC, Courtois Y, Fuhrmann G. Expression of the chicken cystein-rich fibroblast growth factor receptor (CFR) during embryogenesis and retina development. J. Neurosci. Res. 1996;43:602-612.
20. Fennewald SM, Rando RF. Inhibition of high affinity basic fibroblast growth factor binding by oligonucleotides. J. Biol. Chem. 1995;270: 21718-21721.
21. Frade JM, Bovolenta P, Martinez-Moralez JR, Arribas A, Barbas JA, Rodriguez-Tebar A. Control of early cell death by BDNF in the chick retina. Development 1997;124:3313-3320.
22. Fuhrmann S, Kirsch M, Hofmann HD. Ciliary neurotrophic factor promotes chick photoreceptor development in vitro. Development 1995;121:2695-2706.
23. Gao H, Hollyfield JG. Basic fibroblast growth factor in retinal development: Differential levels of bFGF expression and content in normal and retinal degeneration (rd) mutant mice. Dev. Biol. 1995;169:168-184.
24. Gao H, Hollyfield JG. Basic fibroblast growth factor: Increased gene expression in inherited and light-induced photoreceptor degeneration. Exp. Eye Res. 1996;62:181-189.
25. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear fragmentation. J. Cell Biol. 1992;119:493-501.
26. Guillemot F, Cepko CL. Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an in vitro assay of early retinal development. Development 1992;114:743-754.
27. Guvakova MA, Yabukov LA, Vlodavsky I, Tonkinson JL, Stein CA. Phosphorothioate oligodeoxynucleotides bind to basic fibroblast growth factor, inhibit its binding to cell surface receptors, and remove it from low affinity binding sites on extracellular matrix. J. Biol. Chem. 1995;270:2620-2627.
28. Hicks D, Courtois Y. Acidic fibroblast growth factor stimulates opsin levels in retinal photoreceptor cells in vitro. FEBS Lett. 1988;234: 475-479.
29. Hicks D, Courtois Y. Fibroblast growth factor stimulates photoreceptor differentiation in vitro. J. Neurosci. 1992;12:2022-2033.
30. Hughes WF, McLoon SC. Ganglion cell death during normal retinal development in the chick: Comparisons with cell death induced by early target field destruction. Exp. Neurol. 1979;66:587-601.
31. Ilschner SU, Waring P. Fragmentation of DNA in the retina of chicken embryos coincides with retinal ganglion cell death. Biochem. Biophys. Res. Commun. 1992;183:1056-1061.
32. König A, Menzel T, Wrazel S, Rosen A, Al-Katib A, Raveche E, Gabrilove JL. Basic fibroblast growth factor (bFGF) up-regulates the expression of bcl-2 in B cell chronic lymphocytic leukemia cell line resulting in delaying apoptosis. Leukemia 1997;11:258-265.
33. LaVail MM, Faktorovich EG, Hepler JM, Pearson KL, Yasumura D, Matthes MT, Steinberg RH. Basic fibroblast growth factor protects photoreceptors from light-induced degeneration in albino rats. Ann. N.Y. Acad. Sci. 1991;638:341-347.
34. LaVail MM, Unoki K, Yasumura D, Matthes MT, Yancopoulos GD, Steinberg RH. Multiple growth factors, cytokines and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc. Natl. Acad. Sci. USA 1992;89:11249-11253.
35. Léonetti JP, Mechti N, Degols G, Gagnor C, Lebleu B. Intracellular distribution of microinjected antisense oligonucleotides. Proc. Natl. Acad. Sci. USA 1991;88:2702-2706.
36. Levine EM, Roelink H, Turner J, Reh TA. Sonic Hedgehog promotes rod photoreceptor differentiation in mammalian retinal cells in vitro. J. Neurosci. 1997;15:6277-6288.
37. Lezoualc'h F, Seugnet I, Monnier AL, Ghysdael J, Behr JP, Demeneix BA. Inhibition of neurogenic precursor proliferation by antisense α thyroid hormone receptor oligonucleotides. J. Biol. Chem. 1995;270: 12100-12108.
38. Lilien L. Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 1995;377:158-162.
39. Lipton SA, Wagner JA, Madison RD, D'Amore PA. Acidic fibroblast growth factor enhances regeneration of processes by postnatal mammalian retinal ganglion cells in culture. Proc. Natl. Acad. Sci. USA 1988;85:2388-2392.
40. Loke SL, Stein CA, Zhang XH, Mon K, Nakanishi M, Subasinghue C, Cohen JS, Neckers LM. Characterization of oligonucleotide transport into living cells. Proc. Natl. Acad. Sci. USA 1989;86:3474-3478.
41. Mascarelli F, Raulais D, Counis MF, Courtois Y. Characterization of acidic and basic fibroblast growth factors in brain, retina and vitreous chick embryo. Biochem. Biophys. Res. Commun. 1987;146:478-486.
42. McFarlane S, Cornel E, Amaya E, Holt CE. Inhibition of FGF receptor in retinal ganglion cell axons causes errors in target recognition. Neuron 1996;17:245-254.
43. McLoon SC, Barnes RB. Early differentiation of retinal ganglion cells: An axonal protein expressed by premigratory and migrating retinal ganglion cells. J. Neurosci. 1989;9:1424-1432.
44. McWhirter JR, Goulding M, Weiner JA, Chun J, Murre C. A novel fibroblast growth factor gene expressed in the developing nervous system is a downstream target of the chimeric homeodomain oncoprotein E2A-Pbx1. Development 1997;124:3221-3232.
45. Ohuchi H, Koyama E, Myokai F, Nohno T, Shiraga F, Matsuo T, Matsuo N, Tanigushi S, Nogi S. Expression patterns of two fibroblast growth factor receptor genes during early chick eye development. Exp. Eye Res. 1994;58:649-658.
46. Oppenheim RW, Prevette D, Fuller F. The lack of effect of basic and acidic fibroblast growth factors on the naturally occurring death of neurons in the chick embryo. J. Neurosci. 1992;12:2726-2734.
47. Orson FM, Thomas DW, McShan, WM, Kessler DJ, Hogan ME. Oligonucleotide inhibition of Il2Rα mRNA transcription by promoter region collinear triplex formation in lymphocytes. Nucleic Acids Res. 1991;19:3435-3441.
48. Park CM, Hollenberg MJ. Basic fibroblast growth factor induces retinal regeneration in vivo. Dev. Biol. 1989;134:201-205.
49. Park CM, Hollenberg MJ. Induction of retinal regeneration in vivo by growth factors. Dev. Biol. 1991;148:322-333.
50. Philippe JM, Renaud F, Courtois Y, Laurent M. Cloning of multiple chicken FGF1 mRNAs and their differential expression during development of whole embryo and of the lens. DNA Cell Biol. 1996;15:703-715.
51. Pittack C, Jones M, Reh TA. Basic fibroblast growth factor induces retinal pigment epithelium to generate neural retina in vitro. Development 1991;113:577-578.
52. Pittack C, Grunwald GB, Reh TA. Fibroblast growth factors are necessary for neural retina but not pigmented epithelium differentiation in chick embryos. Development 1997;124:805-816.
53. Prada C, Puga J, Lopez-Mendez L, Lopez R, Ramirez G. Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 1991;3:559-565.
54. Renaud F, Oliver L, Desset S, Tassin H, Romquin N, Courtois Y, Laurent M. Up-regulation of aFGF expression in quiescent cells is related to cell survival. J. Cell. Physiol. 1994;158:435-441.
55. Renaud F, Desset S, Oliver L, Gimenez-Gallego G, Van Obberghen E, Courtois Y, Laurent M. The neurotrophic activity of fibroblast growth factor 1 (FGF1) depends on endogenous FGF1 expression and is independent of the mitogen-activated protein kinase cascade pathway. J Biol. Chem. 1996;271:2801-2811.
56. Represa J, Leon Y, Miner C. The int-2 proto-oncogene is responsible for the induction of the inner ear. Nature 1991;353:561-563.
57. Saffel JL, Williams EJ, Mason IJ, Walsh FS, Doherty P. Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 1997;18:231-242.
58. Schnurch H, Risau W. Differentiating and mature neurons express the acidic fibroblast growth factor gene during chick neural development. Development 1991;111:1143-1154.
59. Sensenbrenner M. The neurotrophic activity of fibroblast growth factor. Progr. Neurobiol. 1993;41:683-704.
60. Sievers J, Hausmann B, Unsicker K, Berry M. Fibroblast growth factors promote the survival of adult rat retinal ganglion cells after transection of the optic nerve. Neurosci. Lett. 1987;76:157-162.
61. Smallwood PM, Munoz-Sanjuan I, Tong P, Macke JP, Hendry SHC, Gilbert DJ, Copeland NG, Jenkins NA, Nathans J, Fibroblast growth factor (FGF) homologous factor: New members of the family implicated in nervous system development. Proc. Natl. Acad. Sci. USA 1996;93:9850-9857.
62. Sugi Y, Sasse J, Lough J. Inhibition of precardiac mesoderm cell proliferation by antisense oligodeoxynucleotide complementary to fibroblast growth factor-2 (FGF-2). Dev. Biol. 1993;157:28-37.
63. Svinarchuk F, Debin A, Bertrand JR, Malvy C. Investigation of the intracellular stability and formation of a triple helix formed with a short purine oligonucleotide targeted to the murine c-pim-1 protooncogene promoter. Nucleic Acids Res. 1996;24:295-302.
64. Tcheng M, Fuhrmann G, Hartmann MP, Courtois Y, Jeanny JC. Spatial and temporal expression patterns of FGF receptor genes type 1 and type 2 in the developing chick retina. Exp. Eye Res. 1994a;58:351-358.
65. Tcheng M, Oliver L, Courtois Y, Jeanny JC. Effects of exogenous FGFs on growth, differentiation and survival of chick neural retina cells. Exp. Cell Res. 1994b;212:30-35.
66. Waid DK, McLoon SC. Immediate differentiation of ganglion cells following mitosis in the developing retina. Neuron 1995;14:117-124.
67. Weil M, Jacobson MD, Coles HSR, Davies TJ, Gardner RL, Raff KD, Raff MC. Constitutive expression of the machinery for programmed cell death. J. Cell Biol. 1996;133:1053-1059.
68. Wen R, Song Y, Cheng T, Matthes MT, Yasumura D, LaVail MM, Steinberg RH. Injury-induced up-regulation of bFGF and CNTF mRNAS in the rat retina. J. Neurosci. 1995;15:7377-7385.
69. Yamasaki M, Miyake A, Tagashira S, Itoh N. Structure and expression of the rat mRNA encoding a novel member of the fibroblast growth factor family. J. Biol. Chem. 1996;271:15918-15921.