Sonic hedgehog promotes rod photoreceptor differentiation in mammalian retinal cells in vitro

Journal of Neuroscience

Volumn 17, Issue 16, 1997, Pages 6277-6288

  Levine, Edward M ^a   Roelink, Henk ^a   Turner, Jennifer ^a   Reh, Thomas A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Desert hedgehog; Differentiation; Indian hedgehog; Mitogenesis; Retina; Rod photoreceptor; Sonic hedgehog

Indexed keywords

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; DROSOPHILA; EMBRYO DEVELOPMENT; HEDGEHOG; MITOGENESIS; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA CELL; RETINA DEVELOPMENT;

EID: 0030797144     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-16-06277.1997     Document Type: Article

References (81)

1. Altshuler D, Lo-Turco JJ, Rush J, Cepko C (1993) Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119:1317-1328.
2. Anchan RM, Reh TA (1995) Transforming growth factor-heta-3 is mitogenic for rat retinal progenitor cells in vitro. J Neurobiol 28:133-145.
3. Anchan R, Angello J, Balliet A, Walker M, Reh TA (1991) EGF and TGF stimulate retinal germinal neuroepithelial proliferation. Neuron 6:1-20.
4. Araki M, Iiada Y, Taketami S, Watanabe M, Ohta K, Saito J (1987) Characterization of photoreceptor cell differentiation in the rat retinal cell culture. Dev Biol 124:239-247.
5. Bermingham-McDonogh O, McCabe K, Reh TA (1996) GGF/neuregulins promote neuronal survival and neurite outgrowth in rat retinal cells in vitro. Development 122:1427-1438.
6. Bitgood MJ, McMahon AP (1995) Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 172:126-138.
7. Bugra K, Oliver L, Jacquemin E, Laurent M, Courtois Y, Hicks D (1993) Acidic fibroblast growth factor is expressed abundantly by photoreceptors within the developing and mature rat retina. Eur J Neurosci [Erratum (1994) 6:1062] 5:1586-1595.
8. Bumsted K, Hendrickson A, Erickson A, Szel A (1993) Immunocytochemical development of cone opsins in Macaca monkey retina. Soc Neurosci Abstr 19:52.
9. Cattaneo E, McKay R (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347:762-765.
10. Chang DT, Lopez A, von Kesseler DP, Chiang C, Simandl BK, Renbin Z, Seldin MF, Fallon JF, Beachy PA (1994) Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120:3339-3353.
11. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA (1996) Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383:407-413.
12. Concordet JP, Lewis KE, Moore JW, Goodrich LV, Johnson RL, Scott MP, Ingham PW (1996) Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122:2835-2846.
13. De Leeuw AM, Gaur VP, Saari JC, Milam AH (1990) Immunolocalization of cellular retinol-, retinaldehyde- and retinoic acid-binding proteins in rat retina during pre- and postnatal development. J Neurocytol 19:253-264.
14. Dizhoor AM, Ray S, Kumar S, Niemi G, Spencer M, Brolley D, Walsh KA, Philipov PP, Hurley JB, Stryer L (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 251:915-918.
15. Dorn GM, Hendrickson LE, Hendrickson A (1995) The appearance of rod opsin during monkey retinal development. Invest Ophthalmol Visual Sci 36:2634-2651.
16. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417-1430.
17. Ekker SC, McGrew LL, Lai C-J, Lee JJ, von Kessler DP, Moon RT, Beachy PA (1995a) Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development 121:2337-2347.
18. Ekker SC, Ungar AR, Greenstein P, von-Kessler DP, Porter JA, Moon RT, Beachy PA (1995b) Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol 5:944-955.
19. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, Edlund T (1995) Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell [Erratum (1995) 82:165] 81:747-756.
20. Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM (1996) Two critical periods of long-range sonic hedgehog signalling required for the specification of motor neuron identity. Cell 87:661-673.
21. Ezzeddine ZD, Yang X, DeChiara T, Yancopoulos G, Cepko CL (1997) Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina. Development 124:1055-1067.
22. Fan CM, Porter JA, Chiang C, Chang DT, Beachy PA, Tessier-Lavigne M (1995) Long-range sclerotome induction by sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81:457-465.
23. Felsenfeld AL, Kennison JA (1995) Positional signaling by hedgehog in Drosophila imaginal disc development. Development 121:1-10.
24. Gao H, Hollyfield JG (1995) Basic fibroblast growth factor in retinal development: differential levels of bFGF expression and content in normal and retinal degeneration (rd) mutant mice. Dev Biol 169:168-184.
25. Grondona JM, Kastner P, Gansmuller A, Decimo D, Chambon P (1996) Retinal dysplasia and degeneration in RARβ2/RARγ2 compound mutant mice. Development 122:2173-2188.
26. Hammerschmidt M, Bitgood MJ, McMahon AP (1996) Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev 10:647-658.
27. Harris WA, Messersmith SL (1992) Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron 9:357-372.
28. Hayes KC, Carey RE, Schmidt SY (1975) Retinal degeneration associated with taurine deficiency in the cat. Science 188:949-951.
29. Heberlein U, Singh CM, Luk AY, Donohoe TJ (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373:709-711.
30. Helms J, Thaller C, Eichele G (1994) Relationship between retinoic acid and sonic hedgehog, two polarizing signals in the chick wing bud. Development 120:3267-3274.
31. Hicks D, Barnstable CJ (1987) Different monoclonal antibodies reveal different binding patterns on developing and adult retina. J Histochem Cytochem 35:1317-1328.
32. Hicks D, Courtois Y (1992) Fibroblast growth factor stimulates photoreceptor differentiation in vitro. J Neurosci 12:2022-2033.
33. Holt CE, Bertsch TW, Ellis HM, Harris WA (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15-26.
34. Hunter DD, Murphy MD, Olsson CV, Brunken WJ (1992) S-laminin expression in adult and developing retinae: a potential cue for photoreceptor morphogenesis. Neuron 8:399-413.
35. Hyatt GA, Schmitt EA, Dowling JE (1995) Retinoic acid induces the expansion of rod photoreceptors in the developing zebrafish retina. Soc Neurosci Abstr 21:611.10.
36. Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, Rosenthal A (1995) Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron 15:35-44.
37. Jasoni CL, Reh TA (1996) Temporal and spatial pattern of MASH-1 expression in the developing rat retina demonstrates progenitor cell heterogeneity. J Comp Neurol 368:1-10.
38. Jasoni CL, Walker MB, Morris MD, Reh TA (1994) A chicken achaetescute homolog (CASH-1) is expressed in a temporally and spatially discrete manner in the developing nervous system. Development 120:769-783.
39. Jensen AM, Wallace VA (1997) Expression of Sonic hedgehog and its putative role as a precursor cell mitogen in the developing mouse retina. Development 124:363-371.
40. Jiang J, Struhl G (1995) Protein kinase A and hedgehog signaling in Drosophila limb development. Cell 80:563-572.
41. Johnson RL, Tabin C (1995) The long and short of hedgehog signaling. Cell 81:313-316.
42. Kelley MW, Turner JK, Reh TA (1994) Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120:2091-2102.
43. Kelley MW, Turner JK, Reh TA (1995) Ligands of steroid/thyroid receptors induce cone photoreceptors in vertebrate retina. Development 121:3777-3785.
44. Kirsch M, Fuhrmann S, Wiese A, Hofmann HD (1996) CNTF exerts opposite effects on in vitro development of rat and chick photoreceptors. NeuroReport 7:697-700.
45. Kljavin IJ, Reh TA (1991) Müller cells are a preferred substrate for in vitro neurite extension by rod photoreceptors. J Neurosci 11:2985-2994.
46. Knight JK, Raymond PA (1990) Time course of opsin expression in developing rod photoreceptors. Development 110:1115-1120.
47. Krauss S, Concordet JP, Ingham PW (1993) A functionally conserved homolog of the Drosophila segment polarity gene hedgehog is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75:1431-1444.
48. Lake N (1994) Taurine and GABA in the rat retina during postnatal development. Vis Neurosci 11:253-260.
49. Lee JJ, Ekker SC, von Kessler D, Porter JA, Sun BI, Beachy PA (1994) Autoproteolysis in hedgehog protein biogenesis. Science 266:1528-1537.
50. Li W, Ohlmeyer JT, Lane ME, Kalderon D (1995) Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 80:553-562.
51. Libby RT, Hunter DD, Merlie JP, Sanes JR, Brunken WJ (1995) Characterization of developing mouse retinae lacking S-laminin/laminin β2. Soc Neurosci Abstr 21:21.11.
52. Lillien L, Cepko C (1992) Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF. Development 115:253-266.
53. Liou GI, Wang M, Matragoon S (1994) Timing of interphotoreceptor retinoid-binding protein (IRBP) gene expression and hypomethylation in developing mouse retina. Dev Biol 161:345-356.
54. Ma C, Zhou Y, Beachy PA, Moses K (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75:927-938.
55. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ (1996) Biochemical evidence that Patched is the hedgehog receptor. Nature 384:176-179.
56. Milam AH, Dacey DM, Dizhoor AM (1993) Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10:1-12.
57. Pittack C, Grunwald GB, Reh TA (1997) Fibroblast growth factors are necessary for neural retina but not pigmented epithelium differentiation in chick embryos. Development 124:805-816.
58. Porter JA, von Kessler DP, Ekker SC, Young KE, Lee JJ, Moses K, Beachy PA (1995) The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374:363-366.
59. Rakoczy PE, Humphrey MF, Cavaney DM, Chu Y, Constable IJ (1993) Expression of basic fibroblast growth factor and its receptor in the retina of Royal College of Surgeons rats: a comparative study. Invest Ophthalmol Vis Sci 34:1845-1852.
60. Reh TA (1987) Cell-specific regulation of neuronal production in the larval frog retina. J Neurosci 7:3317-3324.
61. Reh TA (1992a) Cellular interactions determine neuronal phenotypes in rodent retinal cultures. J Neurobiol 23:1067-1083.
62. Reh TA (1992b) Generation of neuronal diversity in the vertebrate retina. In: Determinants of neuronal identity (Shankland M, Macagno ER, eds), pp 433-467. New York: Academic.
63. Reh TA, Cagan RL (1994) Intrinsic and extrinsic signals in the developing vertebrate and fly eyes: viewing vertebrate and invertebrate eyes in the same light. Perspect Dev Neurobiol 2:183-190.
64. Reh TA, Kljavin IJ (1989) Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J Neurosci 9:4179-4189.
65. Reh TA, Tully T (1986) Regulation of tyrosine hydroxylase containing amacrine cell number in larval frog retina. Dev Biol 114:463-469.
66. Reh TA, McCabe K, Kelley MW, Bermingham-McDonogh O (1995) Growth factors in the treatment of degenerative retinal disorders. In: Growth factors as drugs for neurological and sensory disorders, CIBA Foundation Symposium 196 (Bock GR, Goode JA, eds), pp 120-134. New York: Wiley.
67. Riddle RD, Johnson RL, Laufer E, Tabin C (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401-1416.
68. Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Ruiz-i-Altaba A, Tanabe Y, Placzek M, Edlund T, Jessell TM, Dodd J (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76:761-775.
69. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM (1995) Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81:445-455.
70. Sparrow JR, Hicks D, Barnstable CJ (1990) Cell commitment and differentiation in explants of embryonic rat neural retina: comparison with the developmental potential of dissociated retina. Dev Brain Res 51:69-84.
71. Spoerri PE, Ulshafer RJ, Ludwig HC, Allen CB, Kelley KC (1988) Photoreceptor cell development in vitro: influence of pigment epithelium conditioned medium on outer segment differentiation. Eur J Cell Biol 46:362-367.
72. Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, Johnson RL, Scott MP, Pennica D, Goddard A, Phillips H, Noll M, Hooper JE, de Sauvage F, Rosenthal A (1996) The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384:129-134.
73. Strutt DI, Wiersdorff V, Mlodzik M (1995) Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373:705-709.
74. Tabata T, Kornberg TB (1994) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76:89-102.
75. Taylor M, Reh TA (1990) Induction of differentiation of rat retinal, germinal, neuroepithelial cells by dbcAMP. J Neurobiol 21:470-481.
76. Turner DL, Cepko CL (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131-136.
77. Turner EE, Jenne KJ, Rosenfeld MG (1994) Brn-3.2: a Brn-3 related transcription factor with distinctive central nervous system expression and regulation by retinoic acid. Neuron 12:205-218.
78. Watanabe T, Raff MC (1990) Rod photoreceptor development in-vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 4:461-467.
79. Watanabe T, Raff MC (1992) Diffusible rod-promoting signals in the developing rat retina. Development 114:899-906.
80. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142-1145.
81. Xiang M, Zhou L, Macke JP, Yoshioka T, Hendry SH, Eddy RL, Shows TB, Nathans J (1995) The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J Neurosci 7:4762-4785.