Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells

Brain Research

Volumn 1228, Issue , 2008, Pages 27-42

  Dakubo, Gabriel D ^a,b   Beug, Shawn T ^a,b,c   Mazerolle, Chantal J ^a,b   Thurig, Sherry ^a,b   Wang, Yaping ^a,b   Wallace, Valerie A ^a,b,c  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA EYE INSTITUTE   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Ccnd1; Cdc25b; Glia; Hedgehog; Mouse; Optic nerve; Proliferation

Indexed keywords

PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN SECRETION; RETINA GANGLION CELL; STEM CELL;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CDC25 PHOSPHATASES; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYCLINS; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROGLIA; OLIGODENDROGLIA; OPTIC NERVE; RECEPTORS, CELL SURFACE; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ERINACEIDAE; MAMMALIA; MUS; WALLERIA;

EID: 49349108973     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.06.058     Document Type: Article

References (65)

1. Agathocleous M., Locker M., Harris W.A., and Perron M. A general role of hedgehog in the regulation of proliferation. Cell Cycle 6 (2007) 156-159
2. Barres B.A., and Raff M.C. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361 (1993) 258-260
3. Barres B.A., and Raff M.C. Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12 (1994) 935-942
4. Barres B.A., and Raff M.C. Axonal control of oligodendrocyte development. J. Cell Biol. 147 (1999) 1123-1128
5. Barres B.A., Hart I.K., Coles H.S., Burne J.F., Voyvodic J.T., Richardson W.D., and Raff M.C. Cell death in the oligodendrocyte lineage. J. Neurobiol. 23 (1992) 1221-1230
6. Barres B.A., Jacobson M.D., Schmid R., Sendtner M., and Raff M.C. Does oligodendrocyte survival depend on axons?. Curr. Biol. 3 (1993) 489-497
7. Barres B.A., Schmid R., Sendnter M., and Raff M.C. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118 (1993) 283-295
8. Barres B.A., Raff M.C., Gaese F., Bartke I., Dechant G., and Barde Y.A. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367 (1994) 371-375
9. Benazeraf B., Chen Q., Peco E., Lobjois V., Medevielle F., Ducommun B., and Pituello F. Identification of an unexpected link between the Shh pathway and a G2/M regulator, the phosphatase CDC25B. Dev. Biol. 294 (2006) 133-147
10. Burne J.F., and Raff M.C. Retinal ganglion cell axons drive the proliferation of astrocytes in the developing rodent optic nerve. Neuron 18 (1997) 223-230
11. Burne J.F., Staple J.K., and Raff M.C. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J. Neurosci. 16 (1996) 2064-2073
12. Dakubo G.D., and Wallace V.A. Hedgehogs and retinal ganglion cells: organizers of the mammalian retina. Neuroreport 15 (2004) 479-482
13. Dakubo G.D., Wang Y.P., Mazerolle C., Campsall K., McMahon A.P., and Wallace V.A. Retinal ganglion cell-derived sonic hedgehog signaling is required for optic disc and stalk neuroepithelial cell development. Development 130 (2003) 2967-2980
14. de Iongh R., and McAvoy J.W. Distribution of acidic and basic fibroblast growth factors (FGF) in the foetal rat eye: implications for lens development. Growth Factors 6 (1992) 159-177
15. Deiner M.S., Kennedy T.E., Fazeli A., Serafini T., Tessier-Lavigne M., and Sretavan D.W. Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19 (1997) 575-589
16. Duman-Scheel M., Weng L., Xin S., and Du W. Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature 417 (2002) 299-304
17. Fernandez P.A., Tang D.G., Cheng L., Prochiantz A., Mudge A.W., and Raff M.C. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 28 (2000) 81-90
18. Frank-Kamenetsky M., Zhang X.M., Bottega S., Guicherit O., Wichterle H., Dudek H., Bumcrot D., Wang F.Y., Jones S., Shulok J., Rubin L.L., and Porter J.A. Small-molecule modulators of Hedgehog signaling: identification and characterization of Smoothened agonists and antagonists. J. Biol. 1 (2002) 10
19. Fruttiger M., Karlsson L., Hall A.C., Abramsson A., Calver A.R., Bostrom H., Willetts K., Bertold C.H., Heath J.K., Betsholtz C., and Richardson W.D. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126 (1999) 457-467
20. Fruttiger M., Calver A.R., and Richardson W.D. Platelet-derived growth factor is constitutively secreted from neuronal cell bodies but not from axons. Curr. Biol. 10 (2000) 1283-1286
21. Gao L., and Miller R.H. Specification of optic nerve oligodendrocyte precursors by retinal ganglion cell axons. J. Neurosci. 26 (2006) 7619-7628
22. Garcion E., Faissner A., and ffrench-Constant C. Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128 (2001) 2485-2496
23. Horsburgh G.M., and Sefton A.J. The early development of the optic nerve and chiasm in embryonic rat. J. Comp. Neurol. 243 (1986) 547-560
24. Hu M.C., Mo R., Bhella S., Wilson C.W., Chuang P.T., Hui C.C., and Rosenblum N.D. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133 (2006) 569-578
25. Huang Z., Shilo B.Z., and Kunes S. A retinal axon fascicle uses spitz, an EGF receptor ligand, to construct a synaptic cartridge in the brain of Drosophila. Cell 95 (1998) 693-703
26. Huxlin K.R., Sefton A.J., and Furby J.H. The origin and development of retinal astrocytes in the mouse. J. Neurocytol. 21 (1992) 530-544
27. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15 (2001) 3059-3087
28. Ishibashi T., Dakin K.A., Stevens B., Lee P.R., Kozlov S.V., Stewart C.L., and Fields R.D. Astrocytes promote myelination in response to electrical impulses. Neuron 49 (2006) 823-832
29. Jensen A.M., and Wallace V.A. Expression of Sonic hedgehog and its putative role as a precursor cell mitogen in the developing mouse retina. Development 124 (1997) 363-371
30. Juurlink B.H., and Fedoroff S. Differentiation capabilities of mouse optic stalk in isolation of its immediate in vivo environment. Dev. Biol. 78 (1980) 215-221
31. Kenney A.M., and Rowitch D.H. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell Biol. 20 (2000) 9055-9067
32. Kessaris N., Jamen F., Rubin L.L., and Richardson W.D. Cooperation between sonic hedgehog and fibroblast growth factor/MAPK signalling pathways in neocortical precursors. Development 131 (2004) 1289-1298
33. Lai K., Kaspar B.K., Gage F.H., and Schaffer D.V. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6 (2003) 21-27
34. Le Bras B., Barallobre M.J., Homman-Ludiye J., Ny A., Wyns S., Tammela T., Haiko P., Karkkainen M.J., Yuan L., Muriel M.P., Chatzopoulou E., Breant C., Zalc B., Carmeliet P., Alitalo K., Eichmann A., and Thomas J.L. VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat. Neurosci. 9 (2006) 340-348
35. Lewis P.M., Dunn M.P., McMahon J.A., Logan M., Martin J.F., St-Jacques B., and McMahon A.P. Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell 105 (2001) 599-612
36. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
37. Lobjois V., Benazeraf B., Bertrand N., Medevielle F., and Pituello F. Specific regulation of cyclins D1 and D2 by FGF and Shh signaling coordinates cell cycle progression, patterning, and differentiation during early steps of spinal cord development. Dev. Biol. 273 (2004) 195-209
38. Locker M., Agathocleous M., Amato M.A., Parain K., Harris W.A., and Perron M. Hedgehog signaling and the retina: insights into the mechanisms controlling the proliferative properties of neural precursors. Genes Dev. 20 (2006) 3036-3048
39. Lu Q.R., Yuk D., Alberta J.A., Zhu Z., Pawlitzky I., Chan J., McMahon A.P., Stiles C.D., and Rowitch D.H. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25 (2000) 317-329
40. 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
41. Mi H., and Barres B.A. Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J. Neurosci. 19 (1999) 1049-1061
42. Mi H., Haeberle H., and Barres B.A. Induction of astrocyte differentiation by endothelial cells. J. Neurosci. 21 (2001) 1538-1547
43. Mill P., Mo R., Hu M.C., Dagnino L., Rosenblum N.D., and Hui C.C. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev. Cell 9 (2005) 293-303
44. Morcillo J., Martinez-Morales J.R., Trousse F., Fermin Y., Sowden J.C., and Bovolenta P. Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development 133 (2006) 3179-3190
45. Navascues J., Rodriguez-Gallardo L., Martin-Partido G., and Alvarez I.S. Proliferation of glial precursors during the early development of the chick optic nerve. Anat. Embryol. (Berl) 172 (1985) 365-373
46. Noble M., Murray K., Stroobant P., Waterfield M.D., and Riddle P. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333 (1988) 560-562
47. Oliver T.G., Grasfeder L.L., Carroll A.L., Kaiser C., Gillingham C.L., Lin S.M., Wickramasinghe R., Scott M.P., and Wechsler-Reya R.J. Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc. Natl. Acad. Sci. U S A 100 (2003) 7331-7336
48. Pringle N.P., Mudhar H.S., Collarini E.J., and Richardson W.D. PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115 (1992) 535-551
49. Raff M.C., and Lillien L.E. Differentiation of a bipotential glial progenitor cell: what controls the timing and the choice of developmental pathway?. J. Cell Sci. Suppl. 10 (1988) 77-83
50. Raff M.C., Barres B.A., Burne J.F., Coles H.S., Ishizaki Y., and Jacobson M.D. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262 (1993) 695-700
51. Richardson W.D., Pringle N., Mosley M.J., Westermark B., and Dubois-Dalcq M. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53 (1988) 309-319
52. Shi J., Marinovich A., and Barres B.A. Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. J. Neurosci. 18 (1998) 4627-4636
53. Silver J., and Robb R.M. Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Dev. Biol. 68 (1979) 175-190
54. Small R.K., Riddle P., and Noble M. Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328 (1987) 155-157
55. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics 21 (1999) 70-71
56. Spassky N., de Castro F., Le Bras B., Heydon K., Queraud-LeSaux F., Bloch-Gallego E., Chedotal A., Zalc B., and Thomas J.L. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22 (2002) 5992-6004
57. Spence J.R., Madhavan M., Ewing J.D., Jones D.K., Lehman B.M., and Del Rio-Tsonis K. The hedgehog pathway is a modulator of retina regeneration. Development 131 (2004) 4607-4621
58. Sugimoto Y., Taniguchi M., Yagi T., Akagi Y., Nojyo Y., and Tamamaki N. Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 128 (2001) 3321-3330
59. Traiffort E., Moya K.L., Faure H., Hassig R., and Ruat M. High expression and anterograde axonal transport of aminoterminal sonic hedgehog in the adult hamster brain. Eur. J. Neurosci. 14 (2001) 839-850
60. Ueda H., Levine J.M., Miller R.H., and Trapp B.D. Rat optic nerve oligodendrocytes develop in the absence of viable retinal ganglion cell axons. J. Cell. Biol. 146 (1999) 1365-1374
61. Ulshafer R.J., and Clavert A. Cell death and optic fiber penetration in the optic stalk of the chick. J. Morphol. 162 (1979) 67-76
62. Wallace V.A., and Raff M.C. A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve. Development 126 (1999) 2901-2909
63. Wang S., Sdrulla A.D., diSibio G., Bush G., Nofziger D., Hicks C., Weinmaster G., and Barres B.A. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21 (1998) 63-75
64. 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
65. Wang Y., Dakubo G.D., Thurig S., Mazerolle C.J., and Wallace V.A. 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